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Protein regulation of carotenoid binding; gatekeeper and locking amino acid residues in reaction centers of Rhodobacter sphaeroides.

Roszak AW, McKendrick K, Gardiner AT, Mitchell IA, Isaacs NW, Cogdell RJ, Hashimoto H, Frank HA
Structure 12 765-73 (2004)
Related entries: 1rg5, 1rgn

Cited: 27 times
EuropePMC logo PMID: 15130469

Abstract

X-ray diffraction was used to determine high-resolution structures of the reaction center (RC) complex from the carotenoidless mutant, Rb. sphaeroides R-26.1, without or reconstituted with carotenoids. The results are compared with the structure of the RC from a semiaerobically grown Rb. sphaeroides strain 2.4.1. The investigation reveals the structure of the carotenoid in the different protein preparations, the nature of its binding site, and a plausible mechanism by which the carotenoid is incorporated unidirectionally in its characteristic geometric configuration. The structural data suggest that the accessibility of the carotenoid to the binding site is controlled by a specific "gatekeeper" residue which allows the carotenoid to approach the binding site from only one direction. Carotenoid binding to the protein is secured by hydrogen bonding to a separate "locking" amino acid. The study reveals the specific molecular interactions that control how the carotenoid protects the photosynthetic apparatus against photo-induced oxidative destruction.

Reviews citing this publication (5)

  1. Biogenesis, molecular regulation and function of plant isoprenoids. Bouvier F, Rahier A, Camara B. Prog Lipid Res 44 357-429 (2005)
  2. Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs. Kerfeld CA, Melnicki MR, Sutter M, Dominguez-Martin MA. New Phytol 215 937-951 (2017)
  3. Crystal structures of all-alpha type membrane proteins. McLuskey K, Roszak AW, Zhu Y, Isaacs NW. Eur Biophys J 39 723-755 (2010)
  4. Neutron and light scattering studies of light-harvesting photosynthetic antenna complexes. Tang KH, Blankenship RE. Photosynth Res 111 205-217 (2012)
  5. Structure-function investigations of bacterial photosynthetic reaction centers. Leonova MM, Fufina TY, Vasilieva LG, Shuvalov VA. Biochemistry (Mosc) 76 1465-1483 (2011)

Articles citing this publication (22)

  1. Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. Wilson A, Kinney JN, Zwart PH, Punginelli C, D'Haene S, Perreau F, Klein MG, Kirilovsky D, Kerfeld CA. J Biol Chem 285 18364-18375 (2010)
  2. Lipidic sponge phase crystallization of membrane proteins. Wadsten P, Wöhri AB, Snijder A, Katona G, Gardiner AT, Cogdell RJ, Neutze R, Engström S. J Mol Biol 364 44-53 (2006)
  3. Reconstitution of gloeobacter rhodopsin with echinenone: role of the 4-keto group. Balashov SP, Imasheva ES, Choi AR, Jung KH, Liaaen-Jensen S, Lanyi JK. Biochemistry 49 9792-9799 (2010)
  4. Energetic insights into two electron transfer pathways in light-driven energy-converting enzymes. Kawashima K, Ishikita H. Chem Sci 9 4083-4092 (2018)
  5. New insights into the structure of the reaction centre from Blastochloris viridis: evolution in the laboratory. Roszak AW, Moulisová V, Reksodipuro AD, Gardiner AT, Fujii R, Hashimoto H, Isaacs NW, Cogdell RJ. Biochem J 442 27-37 (2012)
  6. Chromophore interaction in xanthorhodopsin--retinal dependence of salinixanthin binding. Imasheva ES, Balashov SP, Wang JM, Smolensky E, Sheves M, Lanyi JK. Photochem Photobiol 84 977-984 (2008)
  7. Percentile-based spread: a more accurate way to compare crystallographic models. Pozharski E. Acta Crystallogr D Biol Crystallogr 66 970-978 (2010)
  8. Two stereoisomers of spheroidene in the Rhodobacter sphaeroides R26 reaction center: a DFT analysis of resonance Raman spectra. Wirtz AC, van Hemert MC, Lugtenburg J, Frank HA, Groenen EJ. Biophys J 93 981-991 (2007)
  9. Removal and reconstitution of the carotenoid antenna of xanthorhodopsin. Imasheva ES, Balashov SP, Wang JM, Lanyi JK. J Membr Biol 239 95-104 (2011)
  10. The conformation of end-groups is one determinant of carotenoid topology suitable for high fidelity molecular recognition: a study of beta- and epsilon-end-groups. Landrum JT, Chatfield DC, Mebel AM, Alvarez-Calderon F, Fernandez MV. Arch Biochem Biophys 493 169-174 (2010)
  11. Triplet state spectra and dynamics of geometric isomers of carotenoids. Pendon ZD, der Hoef I, Lugtenburg J, Frank HA. Photosynth Res 88 51-61 (2006)
  12. Uncovering the interactions driving carotenoid binding in light-harvesting complexes. Mascoli V, Liguori N, Cupellini L, Elias E, Mennucci B, Croce R. Chem Sci 12 5113-5122 (2021)
  13. The role of aromatic phenylalanine residues in binding carotenoid to light-harvesting model and wild-type complexes. García-Martín A, Pazur A, Wilhelm B, Silber M, Robert B, Braun P. J Mol Biol 382 154-166 (2008)
  14. Lipid binding to the carotenoid binding site in photosynthetic reaction centers. Deshmukh SS, Tang K, Kálmán L. J Am Chem Soc 133 16309-16316 (2011)
  15. Probing binding site of bacteriochlorophyll a and carotenoid in the reconstituted LH1 complex from Rhodospirillum rubrum S1 by Stark spectroscopy. Nakagawa K, Suzuki S, Fujii R, Gardiner AT, Cogdell RJ, Nango M, Hashimoto H. Photosynth Res 95 339-344 (2008)
  16. The 17-propionate esterifying variants of bacteriochlorophyll-a and bacteriopheophytin-a in purple photosynthetic bacteria. Mizoguchi T, Isaji M, Harada J, Tsukatani Y, Tamiaki H. J Photochem Photobiol B 142 244-249 (2015)
  17. Comparative ENDOR study at 34 GHz of the triplet state of the primary donor in bacterial reaction centers of Rb. sphaeroides and Bl. viridis. Marchanka A, Lubitz W, Plato M, van Gastel M. Photosynth Res 120 99-111 (2014)
  18. Configuration of spheroidene in the photosynthetic reaction center of Rhodobacter sphaeroides : a comparison of wild-type and reconstituted R26. Mathies G, van Hemert MC, Gast P, Gupta KB, Frank HA, Lugtenburg J, Groenen EJ. J Phys Chem A 115 9552-9556 (2011)
  19. Energy dissipative photoprotective mechanism of carotenoid spheroidene from the photoreaction center of purple bacteria Rhodobacter sphaeroides. Arulmozhiraja S, Nakatani N, Nakayama A, Hasegawa JY. Phys Chem Chem Phys 17 23468-23480 (2015)
  20. Excited-State Dynamics of All the Mono-cis and the Major Di-cis Isomers of β-Apo-8'-Carotenal as Revealed by Femtosecond Time-Resolved Transient Absorption Spectroscopy. Horiuchi K, Uragami C, Tao R, Kosumi D, Cogdell RJ, Hashimoto H. Molecules 28 4424 (2023)
  21. Comment Secrets of carotenoid binding. Tracewell CA. Structure 12 733-734 (2004)
  22. Pigment-modified reaction centers of Chloroflexus aurantiacus: chemical exchange of bacteriopheophytins with plant-type pheophytins. Zabelin AA, Shkuropatov AY. Photosynth Res 149 313-328 (2021)


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