Intrinsic Negative Feedback Governs Activation Surge in Two-Component Regulatory Systems

Molecular Cell

Volumn 45, Issue 3, 2012, Pages 409-421

  Yeo, Won Sik ^a,b,c   Zwir, Igor ^a,b,c,d   Huang, Henry V ^c   Shin, Dongwoo ^c   Kato, Akinori ^c   Groisman, Eduardo A ^a,b,c,e  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF GRANADA   (Spain)

^e YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; MESSENGER RNA; PHOP PROTEIN; PHOQ PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; IN VITRO STUDY; IN VIVO STUDY; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE BINDING SITE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SALMONELLA ENTERICA;

ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; KINETICS; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84863058834     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.12.027     Document Type: Article

References (57)

1. Alloing G., Martin B., Granadel C., Claverys J.P. Development of competence in Streptococcus pneumonaie: pheromone autoinduction and control of quorum sensing by the oligopeptide permease. Mol. Microbiol. 1998, 29:75-83.
2. Alper S., Duncan L., Losick R. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis. Cell 1994, 77:195-205.
3. Bennett B.D., Kimball E.H., Gao M., Osterhout R., Van Dien S.J., Rabinowitz J.D. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 2009, 5:593-599.
4. Bhattacharya A., Kurochkin A.V., Yip G.N., Zhang Y., Bertelsen E.B., Zuiderweg E.R. Allostery in Hsp70 chaperones is transduced by subdomain rotations. J.Mol. Biol. 2009, 388:475-490.
5. Buckstein M.H., He J., Rubin H. Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J.Bacteriol. 2008, 190:718-726.
6. Cai S.J., Inouye M. EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J.Biol. Chem. 2002, 277:24155-24161.
7. Casino P., Rubio V., Marina A. Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 2009, 139:325-336.
8. 2+ regulation of the sensor protein PhoQ in Salmonella. J.Biol. Chem. 2000, 275:22948-22954.
9. Chamnongpol S., Groisman E.A. Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase. J.Mol. Biol. 2000, 300:291-305.
10. Chechik G., Oh E., Rando O., Weissman J., Regev A., Koller D. Activity motifs reveal principles of timing in transcriptional control of the yeast metabolic network. Nat. Biotechnol. 2008, 26:1251-1259.
11. Chen W., Huang X., Komuniecki P.R., Komuniecki R. Molecular cloning, functional expression, and characterization of pyruvate dehydrogenase kinase from anaerobic muscle of the parasitic nematode Ascaris suum. Arch. Biochem. Biophys. 1998, 353:181-189.
12. Davey M.J., Fang L., McInerney P., Georgescu R.E., O'Donnell M. The DnaC helicase loader is a dual ATP/ADP switch protein. EMBO J. 2002, 21:3148-3159.
13. Depardieu F., Courvalin P., Msadek T. A six amino acid deletion, partially overlapping the VanSB G2 ATP-binding motif, leads to constitutive glycopeptide resistance in VanB-type Enterococcus faecium. Mol. Microbiol. 2003, 50:1069-1083.
14. Dong G., Kim Y.I., Golden S.S. Simplicity and complexity in the cyanobacterial circadian clock mechanism. Curr. Opin. Genet. Dev. 2010, 20:619-625.
15. Dutta R., Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 2000, 25:24-28.
16. Dutta R., Qin L., Inouye M. Histidine kinases: diversity of domain organization. Mol. Microbiol. 1999, 34:633-640.
17. Gao R., Stock A.M. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 2009, 63:133-154.
18. Hart Y., Madar D., Yuan J., Bren A., Mayo A.E., Rabinowitz J.D., Alon U. Robust control of nitrogen assimilation by a bifunctional enzyme in E. coli. Mol. Cell 2011, 41:117-127.
19. Hoch J.A., Silhavy T.J. Two-Component Signal Transduction 1995, ASM Press, Washington, DC.
20. Hsing W., Russo F.D., Bernd K.K., Silhavy T.J. Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J.Bacteriol. 1998, 180:4538-4546.
21. Hutchings M.I., Hong H.J., Buttner M.J. The vancomycin resistance VanRS two-component signal transduction system of Streptomyces coelicolor. Mol. Microbiol. 2006, 59:923-935.
22. Igo M.M., Ninfa A.J., Stock J.B., Silhavy T.J. Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev. 1989, 3:1725-1734.
23. Inouye M., Dutta R. Histidine kinases in signal transduction 2003, The Company of Biologists Ltd, San Diego, CA.
24. Kang P.J., Sanson A., Lee B., Park H.O. A GDP/GTP exchange factor involved in linking a spatial landmark to cell polarity. Science 2001, 292:1376-1378.
25. Kato A., Groisman E.A. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev. 2004, 18:2302-2313.
26. Kato M., Chuang J.L., Tso S.C., Wynn R.M., Chuang D.T. Crystal structure of pyruvate dehydrogenase kinase 3 bound to lipoyl domain 2 of human pyruvate dehydrogenase complex. EMBO J. 2005, 24:1763-1774.
27. Kremling A., Heermann R., Centler F., Jung K., Gilles E.D. Analysis of two-component signal transduction by mathematical modeling using the KdpD/KdpE system of Escherichia coli. Biosystems 2004, 78:23-37.
28. Machius M., Chuang J.L., Wynn R.M., Tomchick D.R., Chuang D.T. Structure of rat BCKD kinase: nucleotide-induced domain communication in a mitochondrial protein kinase. Proc. Natl. Acad. Sci. USA 2001, 98:11218-11223.
29. Marina A., Mott C., Auyzenberg A., Hendrickson W.A., Waldburger C.D. Structural and mutational analysis of the PhoQ histidine kinase catalytic domain. Insight into the reaction mechanism. J.Biol. Chem. 2001, 276:41182-41190.
30. Marina A., Waldburger C.D., Hendrickson W.A. Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J. 2005, 24:4247-4259.
31. Markson J.S., O'Shea E.K. The molecular clockwork of a protein-based circadian oscillator. FEBS Lett. 2009, 583:3938-3947.
32. Mascher T., Helmann J.D., Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 2006, 70:910-938.
33. Masuda S., Murakami K.S., Wang S., Anders Olson C., Donigian J., Leon F., Darst S.A., Campbell E.A. Crystal structures of the ADP and ATP bound forms of the Bacillus anti-sigma factor SpoIIAB in complex with the anti-anti-sigma SpoIIAA. J.Mol. Biol. 2004, 340:941-956.
34. Miyashiro T., Goulian M. High stimulus unmasks positive feedback in an autoregulated bacterial signaling circuit. Proc. Natl. Acad. Sci. USA 2008, 105:17457-17462.
35. Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., Kondo T. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation invitro. Science 2005, 308:414-415.
36. Neuhard J., Nygaard P. Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology 1987, 445-473. ASM Press, Washington, DC. J. Ingraham, K. Low, B. Magasanik, M. Schaechter, H. Umbarger (Eds.).
37. Park H.O., Bi E., Pringle J.R., Herskowitz I. Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proc. Natl. Acad. Sci. USA 1997, 94:4463-4468.
38. Perego M., Hoch J.A. Protein aspartate phosphatases control the output of two-component signal transduction systems. Trends Genet. 1996, 12:97-101.
39. Ray J.C., Igoshin O.A. Adaptable functionality of transcriptional feedback in bacterial two-component systems. PLoS Comput. Biol. 2010, 6:e1000676.
40. Russo F.D., Silhavy T.J. The essential tension: opposed reactions in bacterial two-component regulatory systems. Trends Microbiol. 1993, 1:306-310.
41. Rust M.J., Golden S.S., O'Shea E.K. Light-driven changes in energy metabolism directly entrain the cyanobacterial circadian oscillator. Science 2011, 331:220-223.
42. Sanowar S., Le Moual H. Functional reconstitution of the Salmonella typhimurium PhoQ histidine kinase sensor in proteoliposomes. Biochem. J. 2005, 390:769-776.
43. Shin D., Lee E.J., Huang H., Groisman E.A. A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circuit. Science 2006, 314:1607-1609.
44. Shinar G., Milo R., Martínez M.R., Alon U. Input output robustness in simple bacterial signaling systems. Proc. Natl. Acad. Sci. USA 2007, 104:19931-19935.
45. Shinar G., Rabinowitz J.D., Alon U. Robustness in glyoxylate bypass regulation. PLoS Comput. Biol. 2009, 5:e1000297.
46. Stock A.M., Robinson V.L., Goudreau P.N. Two-component signal transduction. Annu. Rev. Biochem. 2000, 69:183-215.
47. Tanaka T., Saha S.K., Tomomori C., Ishima R., Liu D., Tong K.I., Park H., Dutta R., Qin L., Swindells M.B., et al. NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ. Nature 1998, 396:88-92.
48. Thelen J.J., Muszynski M.G., Miernyk J.A., Randall D.D. Molecular analysis of two pyruvate dehydrogenase kinases from maize. J.Biol. Chem. 1998, 273:26618-26623.
49. Thelen J.J., Miernyk J.A., Randall D.D. Pyruvate dehydrogenase kinase from Arabidopsis thaliana: a protein histidine kinase that phosphorylates serine residues. Biochem. J. 2000, 349:195-201.
50. Trajtenberg F., Graña M., Ruétalo N., Botti H., Buschiazzo A. Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase. J.Biol. Chem. 2010, 285:24892-24903.
51. Wynn R.M., Chuang J.L., Cote C.D., Chuang D.T. Tetrameric assembly and conservation in the ATP-binding domain of rat branched-chain alpha-ketoacid dehydrogenase kinase. J.Biol. Chem. 2000, 275:30512-30519.
52. Yamada S., Sugimoto H., Kobayashi M., Ohno A., Nakamura H., Shiro Y. Structure of PAS-linked histidine kinase and the response regulator complex. Structure 2009, 17:1333-1344.
53. Yamamoto K., Ishihama A. Transcriptional response of Escherichia coli to external copper. Mol. Microbiol. 2005, 56:215-227.
54. Yang Y., Inouye M. Intermolecular complementation between two defective mutant signal-transducing receptors of Escherichia coli. Proc. Natl. Acad. Sci. USA 1991, 88:11057-11061.
55. Yang Y., Inouye M. Requirement of both kinase and phosphatase activities of an Escherichia coli receptor (Taz1) for ligand-dependent signal transduction. J.Mol. Biol. 1993, 231:335-342.
56. Zhu Y., Inouye M. The role of the G2 box, a conserved motif in the histidine kinase superfamily, in modulating the function of EnvZ. Mol. Microbiol. 2002, 45:653-663.
57. Zhu Y., Qin L., Yoshida T., Inouye M. Phosphatase activity of histidine kinase EnvZ without kinase catalytic domain. Proc. Natl. Acad. Sci. USA 2000, 97:7808-7813.