Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 50, 2014, Pages 17839-17844

  Rivera Cancel, Giomar ^a   Ko, Wen Huang ^a   Tomchick, Diana R ^a   Correa, Fernando ^a,b   Gardner, Kevin H ^a,b,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c CITY COLLEGE OF NEW YORK   (United States)

Author keywords

Cell signaling; Histidine kinase; Photosensory; Regulation; Two component system

Indexed keywords

ADENOSINE TRIPHOSPHATE; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; HISTIDINE; PROTEIN HISTIDINE KINASE; RIBOFLAVIN; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

ARTICLE; AUTOPHOSPHORYLATION; BACTERIAL CHROMATOPHORE; BACTERIUM; BLUE LIGHT; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME STRUCTURE; ERYTHROBACTER LITORALIS; HYDROGEN BOND; ILLUMINATION; MOLECULAR WEIGHT; NONHUMAN; PHOTOACTIVATION; PHOTOSTIMULATION; PROTEIN BINDING; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLIZATION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; SIZE EXCLUSION CHROMATOGRAPHY; SPHINGOMONADACEAE; X RAY DIFFRACTION;

ERYTHROBACTER LITORALIS; PROKARYOTA;

CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; CRYSTALLIZATION; DIMERIZATION; ESCHERICHIA COLI; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN KINASES; SIGNAL TRANSDUCTION; SPHINGOMONADACEAE; X-RAY DIFFRACTION;

EID: 84919363204     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1413983111     Document Type: Article

References (39)

1. West AH, Stock AM (2001) Histidine kinases and response regulator proteins in twocomponent signaling systems. Trends Biochem Sci 26(6):369-376.
2. Matsushita M, Janda KD (2002) Histidine kinases as targets for new antimicrobial agents. Bioorg Med Chem 10(4):855-867.
3. Bilwes AM, Alex LA, Crane BR, Simon MI (1999) Structure of CheA, a signal-transducing histidine kinase. Cell 96(1):131-141.
4. Marina A, Waldburger CD, Hendrickson WA (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24(24):4247-4259.
5. Surette MG, et al. (1996) Dimerization is required for the activity of the protein histidine kinase CheA that mediates signal transduction in bacterial chemotaxis. J Biol Chem 271(2):939-945.
6. Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133-154.
7. Grebe TW, Stock JB (1999) The histidine protein kinase superfamily. Adv Microb Physiol 41(1962):139-227.
8. Swartz TE, et al. (2007) Blue-light-activated histidine kinases: Two-component sensors in bacteria. Science 317(5841):1090-1093.
9. Taylor BL, Zhulin IB (1999) PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63(2):479-506.
10. Correa F, Ko WH, Ocasio V, Bogomolni RA, Gardner KH (2013) Blue light regulated twocomponent systems: Enzymatic and functional analyses of light-oxygen-voltage (LOV) - histidine kinases and downstream response regulators. Biochemistry 52(27):4656-4666.
11. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774-797.
12. Herrou J, Crosson S (2011) Function, structure and mechanism of bacterial photosensory LOV proteins. Nat Rev Microbiol 9(10):713-723.
13. Halavaty AS, Moffat K (2007) N- and C-terminal flanking regions modulate lightinduced signal transduction in the LOV2 domain of the blue light sensor phototropin 1 from Avena sativa. Biochemistry 46(49):14001-14009.
14. Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301(5639):1541-1544.
15. Harper SM, Christie JM, Gardner KH (2004) Disruption of the LOV-Jalpha helix interaction activates phototropin kinase activity. Biochemistry 43(51):16184-16192.
16. Zayner JP, Antoniou C, Sosnick TR (2012) The amino-terminal helix modulates lightactivated conformational changes in AsLOV2. J Mol Biol 419(1-2):61-74.
17. Casino P, Rubio V, Marina A (2009) Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 139(2):325-336.
18. Yamada S, et al. (2006) The signaling pathway in histidine kinase and the response regulator complex revealed by X-ray crystallography and solution scattering. J Mol Biol 362(1):123-139.
19. Wang C, et al. (2013) Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains. PLoS Biol 11(2):e1001493.
20. Casino P, Miguel-Romero L, Marina A (2014) Visualizing autophosphorylation in histidine kinases. Nat Commun 5:3258.
21. Dago AE, et al. (2012) Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis. Proc Natl Acad Sci USA 109(26):E1733-E1742.
22. Diensthuber RP, Bommer M, Gleichmann T, Möglich A (2013) Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators. Structure 21(7):1127-1136.
23. Crosson S, Moffat K (2002) Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 14(5):1067-1075.
24. Vaidya AT, Chen CH, Dunlap JC, Loros JJ, Crane BR (2011) Structure of a light-activated LOV protein dimer that regulates transcription. Sci Signal 4(184):ra50.
25. Möglich A, Moffat K (2007) Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J Mol Biol 373(1):112-126.
26. Nash AI, Ko WH, Harper SM, Gardner KH (2008) A conserved glutamine plays a central role in LOV domain signal transmission and its duration. Biochemistry 47(52):13842-13849.
27. Jones MA, Feeney KA, Kelly SM, Christie JM (2007) Mutational analysis of phototropin 1 provides insights into the mechanism underlying LOV2 signal transmission. J Biol Chem 282(9):6405-6414.
28. Mechaly AE, Sassoon N, Betton J-M, Alzari PM (2014) Segmental helical motions and dynamical asymmetry modulate histidine kinase autophosphorylation. PLoS Biol 12(1):e1001776.
29. Cheung J, Hendrickson WA (2009) Structural analysis of ligand stimulation of the histidine kinase NarX. Structure 17(2):190-201.
30. Purcell EB, McDonald CA, Palfey BA, Crosson S (2010) An analysis of the solution structure and signaling mechanism of LovK, a sensor histidine kinase integrating light and redox signals. Biochemistry 49(31):6761-6770.
31. Wang LC, Morgan LK, Godakumbura P, Kenney LJ, Anand GS (2012) The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm. EMBO J 31(11):2648-2659.
32. Takala H, et al. (2014) Signal amplification and transduction in phytochrome photosensors. Nature 509(7499):245-248.
33. Möglich A, Ayers RA, Moffat K (2009) Design and signaling mechanism of light-regulated histidine kinases. J Mol Biol 385(5):1433-1444.
34. Etzkorn M, et al. (2008) Plasticity of the PAS domain and a potential role for signal transduction in the histidine kinase DcuS. Nat Struct Mol Biol 15(10):1031-1039.
35. Gleichmann T, Diensthuber RP, Möglich A (2013) Charting the signal trajectory in a light-oxygen-voltage photoreceptor by random mutagenesis and covariance analysis. J Biol Chem 288(41):29345-29355.
36. Albanesi D, et al. (2009) Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Proc Natl Acad Sci USA 106(38):16185-16190.
37. Jacques DA, et al. (2008) Histidine kinase regulation by a cyclophilin-like inhibitor. J Mol Biol 384(2):422-435.
38. Whitten AE, et al. (2007) The structure of the KinA-Sda complex suggests an allosteric mechanism of histidine kinase inhibition. J Mol Biol 368(2):407-420.
39. Mascher T (2014) Bacterial (intramembrane-sensing) histidine kinases: signal transfer rather than stimulus perception. Trends Microbiol 22(10):559-565.