Engineering key components in a synthetic eukaryotic signal transduction pathway

Molecular Systems Biology

Volumn 5, Issue , 2009, Pages

  Antunes, Mauricio S ^a   Morey, Kevin J ^a   Tewari Singh, Neera ^a,c   Bowen, Tessa A ^a   Smith, J Jeff ^b,d   Webb, Colleen T ^a   Hellinga, Homme W ^b   Medford, June I ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d PRECISION BIOSCIENCES   (United States)

Author keywords

PhoB; Response regulator; Signal transduction; Synthetic biology

Indexed keywords

CYTOKININ; OUTER MEMBRANE PROTEIN REGULATOR; PROTEIN HISTIDINE KINASE; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; BETA GLUCURONIDASE; GREEN FLUORESCENT PROTEIN; PHOB PROTEIN, BACTERIA; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; TRANSACTIVATOR PROTEIN;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVATION; EUKARYOTE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE TRANSLOCATION; METABOLIC ENGINEERING; NONHUMAN; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN MODIFICATION; PROTEIN PROCESSING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; ARABIDOPSIS; EUKARYOTIC CELL; GENETIC ENGINEERING; GENETICS; METABOLISM; METHODOLOGY; PLANT ROOT; RHIZOBIUM; STATISTICAL ANALYSIS; SYSTEMS BIOLOGY;

BACTERIA (MICROORGANISMS); EUKARYOTA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; CELL NUCLEUS; CYTOKININS; DATA INTERPRETATION, STATISTICAL; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GENETIC ENGINEERING; GLUCURONIDASE; GREEN FLUORESCENT PROTEINS; PLANT ROOTS; PROMOTER REGIONS, GENETIC; PROTEIN KINASES; RHIZOBIUM; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; TRANS-ACTIVATORS;

EID: 67149113654     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2009.28     Document Type: Article

References (63)

1. Aharoni A, Gaidukov L, Khersonsky O, McQ Gould S, Roodveldt C, Tawfik DS (2005) The 'evolvability' of promiscuous protein functions. Nat Genet 37: 73-76
2. Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot (Lond) 97: 883-893
3. Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56: 1535-1544
4. Antunes MS, Ha S-B, Tewari-Singh N, Morey KJ, Trofka AM, Kugrens P, Deyholos M, Medford JI (2006) A synthetic de-greening gene circuit provides a reporting system that is remotely detectable and has a re-set capacity. Plant Biotechnol J 4: 605-622
5. Appleby JL, Parkinson JS, Bourret RB (1996) Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86: 845-848
6. Bachhawat P, Swapna GV, Montelione GT, Stock AM (2005) Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states. Structure 13: 1353-1363
7. Benfey PN, Ren L, Chua N-H (1989) The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J 8: 2195-2202
8. Bhattacharyya RP, Remenyi A, Yeh BJ, Lim WA (2006) Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 75: 655-680
9. Blanco AG, Sola M, Gomis-Ruth FX, Coll M (2002) Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure (Camb) 10: 701-713
10. Brugiere N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, Niu X, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132: 1228-1240
11. Chen MH, Takeda S, Yamada H, Ishii Y, Yamashino T, Mizuno T (2001) Characterization of the RcsC - YojN - RcsB phosphorelay signaling pathway involved in capsular synthesis in Escherichia coli. Biosci Biotechnol Biochem 65: 2364-2367
12. Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot (Lond) 95: 901-915
13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
14. Dueber JE, Yeh BJ, Bhattacharyya RP, Lim WA (2004) Rewiring cell signaling: the logic and plasticity of eukaryotic protein circuitry. Curr Opin Struct Biol 14: 690-699
15. Ellison DW, McCleary WR (2000) The unphosphorylated receiver domain of PhoB silences the activity of its output domain. J Bacteriol 182: 6592-6597
16. Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8: 518-525
17. Gallagher SR (1992) GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression. San Diego: Academic Press
18. Grefen C, Harter K (2004) Plant two-component systems: principles, functions, complexity and cross talk. Planta 219: 733-742
19. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7: 40-49
20. Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD, Hwang I, Zhu T, Schafer E, Kudla J, Harter K (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23: 3290-3302
21. Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18: 3073-3087
22. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063
23. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: bglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907
24. Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54: 605-627
25. Kjemtrup S, Nimchuk Z, Dangl JL (2000) Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr Opin Microbiol 3: 73-78
26. Koretke KK, Lupas AN, Warren PV, Rosenberg M, Brown JR (2000) Evolution of two-component signal transduction. Mol Biol Evol 17: 1956-1970
27. Kraut DA, Carroll KS, Herschlag D (2003) Challenges in enzyme mechanism and energetics. Annu Rev Biochem 72: 517-571
28. Kuroha T, Ueguchi C, Sakakibara H, Satoh S (2006) Cytokinin receptors are required for normal development of auxin-transporting vascular tissues in the hypocotyl but not in adventitious roots. Plant Cell Physiol 47: 234-243
29. Laub MT, Goulian M (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41: 121-145
30. Looger LL, Dwyer MA, Smith JJ, Hellinga HW (2003) Computational design of receptor and sensor proteins with novel functions. Nature 423: 185-190
31. Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311: 94-98
32. Makino K, Shinagawa H, Amemura M, Kawamoto T, Yamada M, Nakata A (1989) Signal transduction in the phosphate regulon of Escherichia coli involves phosphotransfer between PhoR and PhoB proteins. J Mol Biol 210: 551-559
33. Makino K, Shinagawa H, Amemura M, Nakata A (1986) Nucleotide sequence of the phoB gene, the positive regulatory gene for the phosphate regulon of Escherichia coli K-12. J Mol Biol 190: 37-44
34. Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17: 3007-3018
35. Mizuno T (2005) Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci Biotechnol Biochem 69: 2263-2276
36. Mizuno T, Wurtzel ET, Inouye M (1982) Cloning of the regulatory genes (ompR and envZ) for the matrix proteins of the Escherichia coli outer membrane. J Bacteriol 150: 1462-1466
37. Moore I, Samalova M, Kurup S (2006) Transactivated and chemically inducible gene expression in plants. Plant J 45: 651-683
38. Morey KJ, Tewari-Singh N, Smith JJ, Medford JI (2009) Signal-dependent nuclear shuttling of Arabidopsis histidine phospho-transferases shows cell, tissue and developmental regulation (in preparation)
39. Moritz T, Sundberg B (1996) Endogenous cytokinins in the vascular cambial region of Pinus sylvestris during activity and dormancy. Physiologia Plantarum 98: 693-698
40. Nemecek JC, Wuthrich M, Klein BS (2006) Global control of dimorphism and virulence in fungi. Science 312: 583-588
41. Okamura H, Hanaoka S, Nagadoi A, Makino K, Nishimura Y (2000) Structural comparison of the PhoB and OmpR DNA-binding/ transactivation domains and the arrangement of PhoB molecules on the phosphate box. J Mol Biol 295: 1225-1236
42. Padidam M (2003) Chemically regulated gene expression in plants. Curr Opin Plant Biol 6: 169-177
43. Padidam M, Cao Y (2001) Elimination of transcriptional interference between tandem genes in plant cells. Biotechniques 31: 328-330, 332-334
44. Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC, Saito H (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 'two-component' osmosensor. Cell 86: 865-875
45. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci USA 103: 11081-11085
46. Reiser V, Raitt DC, Saito H (2003) Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J Cell Biol 161: 1035-1040
47. Romanov GA, Spichal L, Lomin SN, Strnad M, Schmulling T (2005) A live cell hormone-binding assay on transgenic bacteria expressing a eukaryotic receptor protein. Anal Biochem 347: 129-134
48. Sanger M, Daubert S, Goodman RM (1990) Characteristics of a strong promoter from figwort mosaic virus: comparison with the analogous 35S promoter from cauliflower mosaic virus and the regulated mannopine synthase promoter. Plant Mol Biol 14: 433-443
49. Santos JL, Shiozaki K (2001) Fungal histidine kinases. Sci STKE 2001: RE1
50. Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O, Goulian M, Laub MT (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133: 1043-1054
51. Spichal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M, Schmulling T (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol 45: 1299-1305
52. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215
53. Sun C, Yang W, Tu LC, Musser SM (2008) Single-molecule measurements of importin alpha/cargo complex dissociation at the nuclear pore. Proc Natl Acad Sci USA 105: 8613-8618
54. Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, Mizuno T (2001) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol 42: 107-113
55. Triezenberg SJ, Kingsbury RC, McKnight SL (1988) Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev 2: 718-729
56. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11: 1743-1754
57. Walthers D, Tran VK, Kenney LJ (2003) Interdomain linkers of homologous response regulators determine their mechanism of action. J Bacteriol 185: 317-324
58. Wolanin PM, Thomason PA, Stock JB (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3: REVIEWS3013
59. Wurtzel ET, Chou MY, Inouye M (1982) Osmoregulation of gene expression. I. DNA sequence of the ompR gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem 257: 13685-13691
60. Xiang C, Han P, Lutz-iger I, Wang K, Oliver DJ (1999) A mini binary vector series for plant transformation. Plant Mol Biol 40: 711-717
61. Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42: 1017-1023
62. Zarrinpar A, Park SH, Lim WA (2003) Optimization of specificity in a cellular protein interaction network by negative selection. Nature 426: 676-680
63. Zhang W, Shi L (2005) Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology 151: 2159-2173