Change in local dynamics of bacteriorhodopsin with retinal isomerization under pressure as studied by fast magic angle spinning NMR

Polymer Journal

Volumn 44, Issue 8, 2012, Pages 863-867

  Kawamura, Izuru ^a   Yamaguchi, Satoru ^b,c   Nishikawa, Hirohide ^a   Tajima, Kana ^a   Horigome, Miyako ^a   Tuzi, Satoru ^b   Saitǒ, Hazime ^b   Naito, Akira ^a  

^a YOKOHAMA NATIONAL UNIVERSITY   (Japan)

^b UNIVERSITY OF HYOGO   (Japan)

^c OKAYAMA UNIVERSITY OF SCIENCE   (Japan)

Author keywords

bacteriorhodopsin; dynamics; fast magic angle spinning; retinal; solid state NMR

Indexed keywords

APPLIED PRESSURE; BACTERIORHODOPSIN; BACTERIORHODOPSIN (BR); BIOMACROMOLECULES; CENTRIFUGAL FORCES; ISOMERIC RATIOS; LOCAL DYNAMICS; MAGIC ANGLE SPINNING NMR; NMR SIGNALS; NMR SPECTRUM; PRESSURE SOURCE; RETINAL; RETINAL ISOMERIZATION; SAMPLE SPINNING; SCHIFF-BASE; SIGNAL INTENSITIES; SOLID STATE NMR;

DYNAMICS; FUNCTIONAL GROUPS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPHTHALMOLOGY;

MAGIC ANGLE SPINNING;

EID: 84864675584     PISSN: 00323896     EISSN: 13490540     Source Type: Journal    
DOI: 10.1038/pj.2012.116     Document Type: Conference Paper

References (37)

1. Judge, P. J. & Watts, A. Recent contributions from solid-state NMR to the understanding of membrane protein structure and function. Curr. Opin. Chem. Biol. 15, 690-695 (2011).
2. Naito, A. Structure elucidation of membrane-associated peptides and proteins in oriented bilayers by solid-state NMR spectroscopy. Solid State Nucl. Magn. Reson. 36, 67-76 (2009).
3. Chimon, S. & Ishii, Y. Capturing intermediate structures of Alzheimer's b-amyloid, Ab (1-40) by solid-state NMR spectroscopy. J. Am. Chem. Soc. 127, 13472-13473 (2005).
4. Asakura, T., Ohgo, K., Komatsu, K., Kanenari, M. & Okuyama, K. Refinement of repeated b-turn structure for silk I conformation of Bombyx mori silk fibroin using 13C solid-state NMR and X-ray diffraction methods. Macromolecules 38, 7397-7403 (2005).
5. Shi, L., Kawamura, I., Jung, K. H., Brown, L. S. & Ladizhansky, V. Conformation of a Seven-helical transmembrane photosensor in the lipid environment. Angew. Chem. Int. Ed. 50, 1302-1305 (2011).
6. Kawamura, I., Degawa, Y., Yamaguchi, S., Nishimura, K., Tuzi, S., Saito , H. & Naito, A. Pressure-induced isomerization of retinal on bacteriorhodopsin as disclosed by fast magic angle spinning NMR. Photochem. Photobiol. 83, 346-350 (2007).
7. Kawamura, I., Kihara, N., Ohmine, M., Nishimura, K., Tuzi, S., Saito , H. & Naito, A. Solid-state NMR studies of two backbone conformations at Tyr185 as a function of retinal configurations in the dark, light, and pressure adapted bacteriorhodopsins. J. Am. Chem. Soc. 129, 1016-1017 (2007).
8. Tomonaga, Y., Hidaka, T., Kawamura, I., Nishio, T., Ohsawa, K., Okitsu, T., Wada, A., Sudo, Y., Kamo, N., Ramamoorthy, A. & Naito, A. An active photoreceptor intermediate revealed by in situ photoirradiated solid-state NMR spectroscopy. Biophys. J. 101, L50-L52 (2011).
9. Luecke, H., Shobert, B., Richter, H. T., Cartailler, J. P. & Lanyi, J. K. Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science 286, 255-261 (1999).
10. Maeda, A., Iwasa, T. & Yoshizawa, T. Isomeric composition of retinal chromophore in dark-adapted bacteriorhodopsin. J. Biochem. 82, 1599-1604 (1977).
11. DeGroot, H. J. M., Harbison, G. S., Herzfeld, J. & Griffin, R. G. Nuclear magnetic resonance study of the Schiff base in bacteriorhodopsin: Counterion effects on the 15N shift anisotropy. Biochemistry 28, 3346-3353 (1989).
12. Kalisky, O., Goldschmidt, C. R. & Ottolenghi, M. On the photocycle and light adaptation of dark-adapted bacteriorhodopsin. Biophys. J. 19, 185-189 (1977).
13. Hofrichter, J., Henry, E. R. & Lozier, R. H. Photocycles of bacteriorhodopsin in lightand dark-adapted purple membrane studied by time-resolved absorption spectroscopy. Biophys. J. 56, 693-706 (1986).
14. Mizuide, N., Shibata, M., Friedman, N., Sheves, M., Belenky, M., Herzfeld, J. & Kandori, H. Structural changes in bacteriorhodopsin following retinal photoisomerization from the 13-cis form. Biochemistry 45, 10674-10681 (2006).
15. Tsuda, M. & Ebrey, T. G. Effect of high pressure on the absorption spectrum and isomeric composition of bacteriorhodopsin. Biophys. J. 30, 149-158 (1980).
16. Schulte, A. & Bradley, L. High-pressure near-infrared raman spectroscopy of bacteriorhodopsin light to dark adaptation. Biophys. J. 69, 1554-1562 (1995).
17. Bryl, K. & Yoshihara, K. Two processes lead to a stable all-trans and 13-cis isomer equilibrium in dark-adapted bacteriorhodopsin; effect of high-pressure on bacteriorhodopsin, bacteriorhodopsin mutant D96N and fluoro-bacteriorhodopsin analogues. Eur. Biophys. J 31, 539-548 (2002).
18. Andrew, E. R., Bradbury, A. & Eades, R. G. Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182, 1659 (1958).
19. Lowe, I. J. Free induction decays of rotating solids. Phys. Rev. Lett. 2, 285-287 (1959).
20. Bertini, I., Luchinat, C., Parigi, G., Ravera, E., Reif, B. & Turano, P. Solid-state NMR of proteins sedimented by ultracentrifugation. Proc. Natl Acad. Sci. 108, 10396-10399 (2011).
21. Kuchel, P. W., Bubb, W. A., Ramadan, S., Chapman, B. E., Philp, D. J., Coen, M., Gready, J. E., Harvey, P. J., McLean, A. J. & Hock, J. 31P MAS-NMR of human erythrocytes: Independence of cell volume from angular velocity. Magn. Reson. Med. 52, 663-668 (2004).
22. Apperley,D. C., Fletton,R. A., Harris,R.K., Lancaster,R.W., Tavener, S. & Threlfall, T. L. Sulfathiazole polymorphism studied by magic-angle spinning NMR. J. Pharm. Sci. 88, 1275-1280 (1999).
23. Zell, M. T., Padden, B. E., Grant, D. J. W., Schroeder, S. A., Wachholder, K. L., Prakash, I. & Munson, E. J. Investigation of polymorphism in aspartame and neotame using solid-state NMR spectroscopy. Tetrahedron 56, 6603-6616 (2000).
24. Xu, M. & Harris, K. D. M. Altering the polymorphic product distribution in a solid-state dehydration process by rapid sample rotation in a solid-state NMR probe. J. Am. Chem. Soc. 127, 10832-10833.
25. Asano, A., Hori, S., Kitamura, M., Nakazawa, C. T. & Kurosu, T. Influence of magic angle spinning on T1 H of SBR studied by solid state 1H NMR. Polym. J. (e-pub ahead of print 7 March 2012; doi:10.138/pj.2012.10).
26. Saito , H. Conformation-dependent 13C chemical shifts: A new means of conformational characterization as obtained by high-resolution solid-state 13C NMR. Magn. Reson. Chem. 24, 835-852 (1986).
27. Saito , H. & Naito, A. NMR studies on fully hydrated membrane proteins, with emphasis on bacteriorhodopsin as a typical and prototype membrane protein. Biochem. Biophys. Acta -Biomembranes 1768, 3145-3161 (2007).
28. Tanio, M., Inoue, S., Yokota, K., Seki, T., Tuzi, S., Needleman, R., Lanyi, J. K., Naito, A. & Saito , H. Long-distance effects of site-directed mutations on backbone conformation in bacteriorhodopsin from solid state NMR of [1-13C]Val-labeled proteins. Biophys. J. 77, 431-442 (1999).
29. Tuzi, S., Tanio, M., Konishi, H., Inoue, S., Naito, A., Needleman, R., Lanyi, J. K. & Saito , H. Location of cation-binding site in the loop between helices F and G of bacteriorhodopsin as studied by 13C NMR. Biophys. J. 76, 1523-1531 (1999).
30. Oesterhelt, D. & Stoeckenius, W. Isolation of the cell membrane of Halobacterium halobium and its function into red and purple membrane. Methods Enzymol. 31, 667-678 (1974).
31. Benett, A. W., Rienstra, C. M., Auger, M., Lakshmi, K. V. & Griffin, R. G. Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103, 6951-6958 (1995).
32. Bielecki, A. & Burum, D. P. Temperature Dependence of 207Pb MAS Spectra of Solid Lead Nitrate. An Accurate, Sensitive Thermometer for Variable-Temperature MAS. J. Magn. Reson. Ser. A. 116, 215-220 (1995).
33. Tuzi, S., Hasegawa, J., Kawaminami, R., Naito, A. & Saito, H. Regio-selective Detection of Dynamic Structure of Transmembrane a-helices as Revealed from 13C NMR spectra of [3-13C]Ala-labeled Bacteriorhodopsin in the Presence of Mn2+ Ion. Biophys. J 81, 425-434 (2001).
34. Yamaguchi, S., Yonebayashi, K., Konishi, H., Tuzi, S., Naito, A., Lanyi, J. K., Needleman, R. & Saito , H. Cytoplasmic surface structure of bacteriorhodopsin consisting of interhelical loops and C-terminal a helix, modified by a variety of environmental factors as studied by 13C NMR. Eur. J. Biochem. 268, 2218-2228 (2001).
35. Shibata, M., Tanimoto, T. & Kandori, H. Water Molecules in Schiff Base Region of Bacteriorhodopsin. J. Am. Chem. Soc. 125, 13312-13313 (2003).
36. Akasaka, K. Highly Fluctuating structures revealed by variable-pressure nuclear magnetic resonance. Biochemistry 42, 10875-10885 (2003).
37. Tuzi, S., Naito, A. & Saito, H. 13C NMR Study on Conformation and Dynamics of the Transmembrane a-Helices, Loops, and C-Terminus of [3-13C]Ala-Labeled Bacteriorhodopsin. Biochemistry 33, 15046-15052 (1994).