Crystal structure of the eukaryotic light-driven proton-pumping rhodopsin, Acetabularia rhodopsin II, from marine alga

Journal of Molecular Biology

Volumn 411, Issue 5, 2011, Pages 986-998

  Wada, Takashi ^a   Shimono, Kazumi ^a,b   Kikukawa, Takashi ^c   Hato, Masakatsu ^a   Shinya, Naoko ^a   Kim, So Young ^d   Kimura Someya, Tomomi ^a   Shirouzu, Mikako ^a   Tamogami, Jun ^b,c   Miyauchi, Seiji ^b   Jung, Kwang Hwan ^d   Kamo, Naoki ^b   Yokoyama, Shigeyuki ^a,e  

^a RIKEN   (Japan)

^b MATSUYAMA UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d Sogang University   (South Korea)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

cell free protein synthesis; lipidic mesophase; microbial rhodopsin; proton transfer; proton releasing residues

Indexed keywords

ACETABULARIA RHODOPSIN II; ARGININE; ASPARTIC ACID; BACTERIORHODOPSIN; CARBOXYL GROUP; CYSTEINE; GLUTAMIC ACID; HYDROGEN; LEUCINE; PROTON; PROTON PUMP; RHODOPSIN; SCHIFF BASE; SERINE; THIOL GROUP; UNCLASSIFIED DRUG; WATER;

ACETABULARIA; ALGA; AMINO ACID SEQUENCE; ANABAENA; ANIMAL CELL; ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; EUKARYOTE; EXTRACELLULAR MATRIX; HYDROGEN BOND; LIGHT DARK CYCLE; MARINE SPECIES; MOLECULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOCHEMISTRY; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTON TRANSPORT; SIGNAL TRANSDUCTION;

ACETABULARIA; ACETABULARIA ACETABULUM; ALGAE; ANABAENA; EUKARYOTA;

EID: 80051671422     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.06.028     Document Type: Article

References (72)

1. Oesterhelt D., and Stoeckenius W. Functions of a new photoreceptor membrane Proc. Natl Acad. Sci. USA 70 1973 2853 2857
2. Spudich J.L., and Jung K.-H. Microbial Rhodopsins: Phylogenetic and Functional Diversity W.R. Briggs, J.L. Spudich, Handbook of Photosensory Receptors 2005 Wiley-VCH Verlag GmbH & Co. KGaA Weinheim, Germany 1 23
3. Bieszke J.A., Spudich E.N., Scott K.L., Borkovich K.A., and Spudich J.L. A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment Biochemistry 38 1999 14138 14145
4. Béjà O., Aravind L., Koonin E.V., Suzuki M.T., Hadd A., and Nguyen L.P. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea Science 289 2000 1902 1906
5. Adrian L., Ouyang Z., Tseng Y.-Y., and Liang J. Evolutionary pattern of retinal-binding pockets of type I rhodopsin and their functions Photochem. Photobiol. 82 2006 1426 1435 (Pubitemid 46158829)
6. Jung K.-H. The distinct signaling mechanism of microbial sensory rhodopsins in Archaea, Eubacteria and Eukarya Photochem. Photobiol. 83 2007 63 69 (Pubitemid 46697224)
7. Spudich J.L., Yang C.-S., Jung K.-H., and Spudich E.N. Retinylidene proteins: structures and functions from archaea to humans Annu. Rev. Cell Dev. Biol. 16 2000 365 392 (Pubitemid 32037511)
8. Nagel G., Szellas T., Kateriya S., Adeishvili N., Hegemann P., and Bamberg E. Channelrhodopsins: directly light-gated cation channels Biochem. Soc. Trans. 33 2005 863 866 (Pubitemid 41160880)
9. Lanyi J.K. Proton transfers in the bacteriorhodopsin photocycle Biochim. Biophys. Acta 1757 2006 1012 1018 (Pubitemid 44427748)
10. Duschl A., Lanyi J.K., and Zimányi L. Properties and photochemistry of a halorhodopsin from the haloalkalophile, Natronobacterium pharaonis J. Biol. Chem. 265 1990 1261 1267
11. Jung K.-H., Trivedi V.D., and Spudich J.L. Demonstration of a sensory rhodopsin in eubacteria Mol. Microbiol. 47 2003 1513 1522 (Pubitemid 36363336)
12. Sudo Y., Iwamoto M., Shimono K., Sumi M., and Kamo N. Photo-induced proton transport of pharaonis phoborhodopsin (sensory rhodopsin II) is ceased by association with the transducer Biophys. J. 80 2001 916 922 (Pubitemid 32128342)
13. Bamann C., Nagel G., and Bamberg E. Microbial rhodopsins in the spotlight Curr. Opin. Neurobiol. 20 2010 610 616
14. Zhang F., Gradinaru V., Adamantidis A.R., Durand R., Airan R.D., de Lecea L., and Deisseroth K. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures Nat. Protoc. 5 2010 439 456
15. Zhang F., Wang L.-P., Brauner M., Liewald J.F., Kay K., and Watzke N. Multimodal fast optical interrogation of neural circuitry Nature 446 2007 633 639 (Pubitemid 46606891)
16. Chow B.Y., Han X., Dobry A.S., Qian X., Chuong A.S., and Li M. High-performance genetically targetable optical neural silencing by light-driven proton pumps Nature 463 2010 98 102
17. Gradinaru V., Zhang F., Ramakrishnan C., Mattis J., Prakash R., and Diester I. Molecular and cellular approaches for diversifying and extending optogenetics Cell 141 2010 154 165
18. Hirai T., Subramaniam S., and Lanyi J.K. Structural snapshots of conformational changes in a seven-helix membrane protein: lessons from bacteriorhodopsin Curr. Opin. Struct. Biol. 19 2009 433 439
19. Wise K.J., Gillespie N.B., Stuart J.A., Krebs M.P., and Birge R.R. Optimization of bacteriorhodopsin for bioelectronic devices Trends Biotechnol. 20 2002 387 394 (Pubitemid 34880174)
20. Roy S., Kikukawa T., Sharma P., and Kamo N. All-optical switching in pharaonis phoborhodopsin protein molecules IEEE Trans. Nanobioscience 5 2006 178 187 (Pubitemid 44376131)
21. Luecke H., Schobert B., Richter H.T., Cartailler J.P., and Lanyi J.K. Structure of bacteriorhodopsin at 1.55 Å resolution J. Mol. Biol. 291 1999 899 911
22. Royant A., Nollert P., Edman K., Neutze R., Landau E.M., Pebay-Peyroula E., and Navarro J. X-ray structure of sensory rhodopsin II at 2.1-Å resolution Proc. Natl Acad. Sci. USA 98 2001 10131 10136 (Pubitemid 32802986)
23. Kouyama T., Kanada S., Takeguchi Y., Narusawa A., Murakami M., and Ihara K. Crystal structure of the light-driven chloride pump halorhodopsin from Natronomonas pharaonis J. Mol. Biol. 396 2010 564 579
24. Vogeley L., Sineshchekov O.A., Trivedi V.D., Sasaki J., Spudich J.L., and Luecke H. Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å Science 306 2004 1390 1393 (Pubitemid 39532519)
25. Luecke H., Schobert B., Stagno J., Imasheva E.S., Wang J.M., Balashov S.P., and Lanyi J.K. Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore Proc. Natl Acad. Sci. USA 105 2008 16561 16565
26. Schilde C. Rapid photoelectric effect in the algae Acetabularia Z. Naturforsch. T.b 23 1968 1369 1376
27. +-pumping rhodopsin from the marine alga Acetabularia Biophys. J. 91 2006 1471 1479 (Pubitemid 44174264)
28. Shimono K., Goto M., Kikukawa T., Miyauchi S., Shirouzu M., Kamo N., and Yokoyama S. Production of functional bacteriorhodopsin by an Escherichia coli cell-free protein synthesis system supplemented with steroid detergent and lipid Protein Sci. 18 2009 2160 2171
29. Tamogami J., Kikukawa T., Miyauchi S., Muneyuki E., and Kamo N. A tin oxide transparent electrode provides the means for rapid time-resolved pH measurements: application to photoinduced proton transfer of bacteriorhodopsin and proteorhodopsin Photochem. Photobiol. 85 2009 578 589
30. Wang W.-W., Sineshchekov O.A., Spudich E.N., and Spudich J.L. Spectroscopic and photochemical characterization of a deep ocean proteorhodopsin J. Biol. Chem. 278 2003 33985 33991 (Pubitemid 37553234)
31. Shimono K., and Kamo N. Amino acid residues regulating the color among archaeal rhodopsins Recent Res. Dev. Photochem. Photobiol. 7 2004 19 38
32. Nielsen M.B. Model systems for understanding absorption tuning by opsin proteins Chem. Soc. Rev. 38 2009 913 924
33. Spudich J.L. The multitalented microbial sensory rhodopsins Trends Microbiol. 376 2006 480 487 (Pubitemid 44537810)
34. Iwamoto M., Hasegawa C., Sudo Y., Shimono K., Araiso T., and Kamo N. Proton release and uptake of pharaonis phoborhodopsin (sensory rhodopsin II) reconstituted into phospholipids Biochemistry 43 2004 3195 3203 (Pubitemid 38352268)
35. Balashov S.P. Protonation reactions and their coupling in bacteriorhodopsin Biochim. Biophys. Acta 1460 2000 75 94
36. Brown L.S., Dioumaev A.K., Lanyi J.K., Spudich E.N., and Spudich J.L. Photochemical reaction cycle and proton transfers in Neurospora rhodopsin J. Biol. Chem. 276 2001 32495 32505
37. Waschuk S.A., Bezerra A.G. Jr, Shi L., and Brown L.S. Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote Proc. Natl Acad. Sci. USA 102 2005 6879 6883 (Pubitemid 40675410)
38. Dioumaev A.K., Brown L.S., Shih J., Spudich E.N., Spudich J.L., and Lanyi J.K. Proton transfers in the photochemical reaction cycle of proteorhodopsin Biochemistry 41 2002 5348 5358 (Pubitemid 34429369)
39. Ming M., Lu M., Balashov S.P., Ebrey T.G., Li Q., and Ding J. pH dependence of light-driven proton pumping by an archaerhodopsin from Tibet: comparison with bacteriorhodopsin Biophys. J. 90 2006 3322 3332
40. Brown L.S., Sasaki J., Kandori H., Maeda A., Needleman R., and Lanyi J.K. Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin J. Biol. Chem. 270 1995 27122 27126
41. Balashov S.P., Imasheva E.S., Ebrey T.G., Chen N., Menick D.R., and Crouch R.K. Glutamate-194 to cysteine mutation inhibits fast light-induced proton release in bacteriorhodopsin Biochemistry 36 1997 8671 8676 (Pubitemid 27342511)
42. Caffrey M., and Cherezov V. Crystallizing membrane proteins using lipidic mesophases Nat. Protoc. 4 2009 706 731
43. Holm L., Kaariainen S., Rosenstrom P., and Schenkel A. Searching protein structure databases with DaliLite v.3 Bioinformatics 24 2008 2780 2781 (Pubitemid 352722625)
44. Neutze R., Pebay-Peyroula E., Edman K., Royant A., Navarro J., and Landau E.M. Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport Biochim. Biophys. Acta 1565 2002 144 167 (Pubitemid 35284472)
45. Shibata M., Yamashita H., Uchihashi T., Kandori H., and Ando T. High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin Nat. Nanotechnol. 5 2010 208 212
46. Wegener A.A., Chizhov I., Engelhard M., and Steinhoff H.J. Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II.J. Mol. Biol. 301 2000 881 891
47. Yoshida H., Sudo Y., Shimono K., Iwamoto M., and Kamo N. Transient movement of helix F revealed by photo-induced inactivation by reaction of a bulky SH-reagent to cysteine-introduced pharaonis phoborhodopsin (sensory rhodopsin II) Photochem. Photobiol. Sci. 3 2004 537 542 (Pubitemid 38968065)
48. Shimono K., Ikeura Y., Sudo Y., Iwamoto M., and Kamo N. Environment around the chromophore in pharaonis phoborhodopsin: mutation analysis of the retinal binding site Biochim. Biophys. Acta 1515 2001 92 100 (Pubitemid 33086826)
49. Shimono K., Ikeura Y., Sudo Y., Iwamoto M., and Kamo N. Importance of the location of the negative-charged counter-ion against the protonated Schiff base on the chromophore configuration of pharaonis phoborhodopsin J. Photosci. 9 2002 302 304
50. Shimono K., Hayashi T., Ikeura Y., Sudo Y., Iwamoto M., and Kamo N. Importance of the broad regional interaction for spectral tuning in Natronobacterium pharaonis phoborhodopsin (sensory rhodopsin II) J. Biol. Chem. 278 2003 23882 23889 (Pubitemid 36830215)
51. Greenhalgh D.A., Fareens D.L., Subramaniam S., and Khorana H.G. Hydrophobic amino acids in the retinal-binding pocket of bacteriorhodopsin J. Biol. Chem. 268 1993 20305 20311 (Pubitemid 23278937)
52. Ihara K., Amemiya T., Miyashita Y., and Mukohata Y. Met-145 is a key residue in the dark adaptation of bacteriorhodopsin homologs Biophys. J. 67 1994 1187 1191 (Pubitemid 24272971)
53. Luecke H., Richter H.T., and Lanyi J.K. Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution Science 280 1998 1934 1937 (Pubitemid 28299400)
54. Phatak P., Ghosh N., Yu H., Cui Q., and Elstner M. Amino acids with an intermolecular proton bond as proton storage site in bacteriorhodopsin Proc. Natl Acad. Sci. USA 105 2008 19672 19677
55. Zimányi L., Varo G., Chang M., Ni B., Needleman R., and Lanyi J.K. Pathways of proton release in the bacteriorhodopsin photocycle Biochemistry 31 1992 8535 8543
56. Balashov S.P., Imasheva E.S., Govindjee R., and Ebrey T.G. Titration of aspartate-85 in bacteriorhodopsin: what it says about chromophore isomerization and proton release Biophys. J. 70 1996 473 481 (Pubitemid 26021486)
57. Luecke H., Schobert B., Richter H.T., Cartailler J.P., and Lanyi J.K. Structural changes in bacteriorhodopsin during ion transport at 2 Å resolution Science 286 1999 255 260 (Pubitemid 29484682)
58. Shi L., Yoon S.R., Bezerra A.G. Jr, Jung K.H., and Brown L.S. Cytoplasmic shuttling of protons in Anabaena sensory rhodopsin: implications for signaling mechanism J. Mol. Biol. 358 2006 686 700
59. Kawanabe A., Furutani Y., Jung K.H., and Kandori H. Engineering an inward proton transport from a bacterial sensor rhodopsin J. Am. Chem. Soc. 131 2009 16439 16444
60. Kawanabe A., Furutani Y., Jung K.H., and Kandori H. An inward proton transport using Anabaena sensory rhodopsin J. Microbiol. 49 2010 1 6
61. Schneider S.U., Leible M.B., and Yang X.-P. Strong homology between the small subunit of ribulose-1,5-biphosphatecarboxylase/oxygenase of two species of Acetabularia and the occurrence of unusual codon usage Mol. Gen. Genet. 218 1989 445 452
62. - pump activity Biophys. J. 92 2007 2559 2569 (Pubitemid 46536437)
63. He F., Saito K., Kobayashi N., Harada T., Watanabe S., and Kigawa T. Structural and functional characterization of the NHR1 domain of the Drosophila neuralized E3 ligase in the notch signaling pathway J. Mol. Biol. 393 2009 478 495
64. Gill S.C., and Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326 (Pubitemid 19277112)
65. Sato M., Kubo M., Aizawa T., Kamo N., Kikukawa T., Nitta K., and Demura M. Role of putative anion-binding sites in cytoplasmic and extracellular channels of Natronomonas pharaonis halorhodopsin Biochemistry 44 2005 4775 4784 (Pubitemid 40396756)
66. Landau E.M., and Rosenbush J.P. Lipidic cubic phases: a novel concept for the crystallization of membrane proteins Proc. Natl Acad. Sci. USA 93 1996 14532 14535 (Pubitemid 26419001)
67. Hato M., Yamashita I., Kato T., and Abe Y. Aqueous phase behavior of a 1-O-phytanyl-β-d-xyloside/water system. Glycolipid-based bicontinuous cubic phases of crystallographic space groups Pn3m and Ia3d Langmuir 20 2004 11366 11373 (Pubitemid 40049606)
68. Hato M., Yamashita J., and Shiono M. Aqueous phase behavior of lipids with isoprenoid type hydrophobic chains J. Phys. Chem. B 113 2009 10196 10209
69. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326 (Pubitemid 27085611)
70. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
71. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., and Grosse-Kunstleve R.W. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 1998 905 921
72. Emsley P., Lohkamp B., Scott W.G., and Cowtan K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501