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A structural pathway for signaling in the E46Q mutant of photoactive yellow protein.

Rajagopal S, Anderson S, Srajer V, Schmidt M, Pahl R, Moffat K
Structure 13 55-63 (2005)
Related entries: 1t18, 1t19, 1t1a, 1t1b

Cited: 36 times
EuropePMC logo PMID: 15642261

Abstract

In the bacterial photoreceptor photoactive yellow protein (PYP), absorption of blue light by its chromophore leads to a conformational change in the protein associated with differential signaling activity, as it executes a reversible photocycle. Time-resolved Laue crystallography allows structural snapshots (as short as 150 ps) of high crystallographic resolution (approximately 1.6 A) to be taken of a protein as it functions. Here, we analyze by singular value decomposition a comprehensive time-resolved crystallographic data set of the E46Q mutant of PYP throughout the photocycle spanning 10 ns-100 ms. We identify and refine the structures of five distinct intermediates and provide a plausible chemical kinetic mechanism for their inter conversion. A clear structural progression is visible in these intermediates, in which a signal generated at the chromophore propagates through a distinct structural pathway of conserved residues and results in structural changes near the N terminus, over 20 A distant from the chromophore.

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Reviews citing this publication (6)

  1. Structure and signaling mechanism of Per-ARNT-Sim domains. Möglich A, Ayers RA, Moffat K. Structure 17 1282-1294 (2009)
  2. Advances in kinetic protein crystallography. Bourgeois D, Royant A. Curr Opin Struct Biol 15 538-547 (2005)
  3. HERG potassium channel regulation by the N-terminal eag domain. Gustina AS, Trudeau MC. Cell Signal 24 1592-1598 (2012)
  4. A short history of structure based research on the photocycle of photoactive yellow protein. Schmidt M. Struct Dyn 4 032201 (2017)
  5. Time-resolved x-ray crystallography of heme proteins. Srajer V, Royer WE. Methods Enzymol 437 379-395 (2008)
  6. Synergy within structural biology of single crystal optical spectroscopy and X-ray crystallography. De la Mora-Rey T, Wilmot CM. Curr Opin Struct Biol 17 580-586 (2007)

Articles citing this publication (26)

  1. Volume-conserving trans-cis isomerization pathways in photoactive yellow protein visualized by picosecond X-ray crystallography. Jung YO, Lee JH, Kim J, Schmidt M, Moffat K, Srajer V, Ihee H. Nat Chem 5 212-220 (2013)
  2. Watching a signaling protein function in real time via 100-ps time-resolved Laue crystallography. Schotte F, Cho HS, Kaila VR, Kamikubo H, Dashdorj N, Henry ER, Graber TJ, Henning R, Wulff M, Hummer G, Kataoka M, Anfinrud PA. Proc Natl Acad Sci U S A 109 19256-19261 (2012)
  3. Photochemical tools to study dynamic biological processes. Specht A, Bolze F, Omran Z, Nicoud JF, Goeldner M. HFSP J 3 255-264 (2009)
  4. PAS domain allostery and light-induced conformational changes in photoactive yellow protein upon I2 intermediate formation, probed with enhanced hydrogen/deuterium exchange mass spectrometry. Brudler R, Gessner CR, Li S, Tyndall S, Getzoff ED, Woods VL. J Mol Biol 363 148-160 (2006)
  5. Hydrogen bond dynamics in the active site of photoactive yellow protein. Sigala PA, Tsuchida MA, Herschlag D. Proc Natl Acad Sci U S A 106 9232-9237 (2009)
  6. Influence of the crystalline state on photoinduced dynamics of photoactive yellow protein studied by ultraviolet-visible transient absorption spectroscopy. Yeremenko S, van Stokkum IH, Moffat K, Hellingwerf KJ. Biophys J 90 4224-4235 (2006)
  7. Structure-based design of a photocontrolled DNA binding protein. Morgan SA, Al-Abdul-Wahid S, Woolley GA. J Mol Biol 399 94-112 (2010)
  8. pH dependence of the photoactive yellow protein photocycle investigated by time-resolved crystallography. Tripathi S, Srajer V, Purwar N, Henning R, Schmidt M. Biophys J 102 325-332 (2012)
  9. Laue crystal structure of Shewanella oneidensis cytochrome c nitrite reductase from a high-yield expression system. Youngblut M, Judd ET, Srajer V, Sayyed B, Goelzer T, Elliott SJ, Schmidt M, Pacheco AA. J Biol Inorg Chem 17 647-662 (2012)
  10. Predicting the signaling state of photoactive yellow protein. Vreede J, Crielaard W, Hellingwerf KJ, Bolhuis PG. Biophys J 88 3525-3535 (2005)
  11. The transient accumulation of the signaling state of photoactive yellow protein is controlled by the external pH. Borucki B, Joshi CP, Otto H, Cusanovich MA, Heyn MP. Biophys J 91 2991-3001 (2006)
  12. Binding, tuning and mechanical function of the 4-hydroxy-cinnamic acid chromophore in photoactive yellow protein. van der Horst MA, Arents JC, Kort R, Hellingwerf KJ. Photochem Photobiol Sci 6 571-579 (2007)
  13. Neutron and X-ray structural studies of short hydrogen bonds in photoactive yellow protein (PYP). Fisher SZ, Anderson S, Henning R, Moffat K, Langan P, Thiyagarajan P, Schultz AJ. Acta Crystallogr D Biol Crystallogr 63 1178-1184 (2007)
  14. Combined probes of X-ray scattering and optical spectroscopy reveal how global conformational change is temporally and spatially linked to local structural perturbation in photoactive yellow protein. Kim TW, Yang C, Kim Y, Kim JG, Kim J, Jung YO, Jun S, Lee SJ, Park S, Kosheleva I, Henning R, van Thor JJ, Ihee H. Phys Chem Chem Phys 18 8911-8919 (2016)
  15. Ultrafast X-Ray Crystallography and Liquidography. Ki H, Oang KY, Kim J, Ihee H. Annu Rev Phys Chem 68 473-497 (2017)
  16. Hydrogen-bond network probed by time-resolved optoacoustic spectroscopy: photoactive yellow protein and the effect of E46Q and E46A mutations. Losi A, Gensch T, van der Horst MA, Hellingwerf KJ, Braslavsky SE. Phys Chem Chem Phys 7 2229-2236 (2005)
  17. Preparation of large crystals of photoactive yellow protein for neutron diffraction and high resolution crystal structure analysis. Yamaguchi S, Kamikubo H, Shimizu N, Yamazaki Y, Imamoto Y, Kataoka M. Photochem Photobiol 83 336-338 (2007)
  18. 2StrucCompare: a webserver for visualizing small but noteworthy differences between protein tertiary structures through interrogation of the secondary structure content. Drew ED, Janes RW. Nucleic Acids Res 47 W477-W481 (2019)
  19. A conserved helical capping hydrogen bond in PAS domains controls signaling kinetics in the superfamily prototype photoactive yellow protein. Kumauchi M, Kaledhonkar S, Philip AF, Wycoff J, Hara M, Li Y, Xie A, Hoff WD. J Am Chem Soc 132 15820-15830 (2010)
  20. Crystallization of Photosystem II for Time-Resolved Structural Studies Using an X-ray Free Electron Laser. Coe J, Kupitz C, Basu S, Conrad CE, Roy-Chowdhury S, Fromme R, Fromme P. Methods Enzymol 557 459-482 (2015)
  21. Early and efficient induction of antioxidant defense system in Mytilus galloprovincialis embryos exposed to metals and heat stress. Boukadida K, Cachot J, Clérandeaux C, Gourves PY, Banni M. Ecotoxicol Environ Saf 138 105-112 (2017)
  22. Time-resolved spectroscopy of dye-labeled photoactive yellow protein suggests a pathway of light-induced structural changes in the N-terminal cap. Hoersch D, Otto H, Cusanovich MA, Heyn MP. Phys Chem Chem Phys 11 5437-5444 (2009)
  23. Helix formation is a dynamical bottleneck in the recovery reaction of Photoactive Yellow Protein. Vreede J, Hellingwerf KJ, Bolhuis PG. Proteins 72 136-149 (2008)
  24. Comment Resolving protein structure dynamically. Yeremenko S, Hellingwerf KJ. Structure 13 4-6 (2005)
  25. Biological function investigated by time-resolved structure determination. Schmidt M. Struct Dyn 10 010901 (2023)
  26. Reconstruction of ARNT PAS-B Unfolding Pathways by Steered Molecular Dynamics and Artificial Neural Networks. Motta S, Pandini A, Fornili A, Bonati L. J Chem Theory Comput 17 2080-2089 (2021)


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