Solution structures of the core light-harvesting α and β polypeptides from rhodospirillum rubrum: Implications for the pigment-protein and protein-protein interactions

Journal of Molecular Biology

Volumn 347, Issue 2, 2005, Pages 465-477

  Wang, Zheng Yu ^a   Gokan, Kazutaka ^a   Kobayashi, Masayuki ^a   Nozawa, Tsunenori ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

GxxxG motif; Membrane protein; Photosynthesis; Pigment binding; Transmembrane helix

Indexed keywords

AMIDE; AMINO ACID; HISTIDINE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN SUBUNIT;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; HYDROGEN BOND; LIGHT HARVESTING SYSTEM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RHODOSPIRILLUM RUBRUM; WILD TYPE; X RAY CRYSTALLOGRAPHY;

EID: 14644440750     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.01.017     Document Type: Article

References (70)

1. J. Deisenhofer, O. Epp, K. Miki, R. Huber, and H. Michel Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution Nature 318 1985 618 624
2. J.P. Allen, G. Feher, T.O. Yeates, H. Komiya, and D.C. Rees Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors Proc. Natl Acad. Sci. USA 84 1987 5730 5734
3. G. McDermott, D.M. Prince, A.A. Freer, A.M. Hawthornthwaite-Lawless, M.Z. Papiz, R.J. Cogdell, and N.W. Isaac Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria Nature 374 1995 517 521
4. J. Koepke, X. Hu, C. Muenke, K. Schulten, and H. Michel The crystal structure of the light-harvesting complex II (B800-B850) from Rhodospirillum molischianum Structure 4 1996 581 597
5. S. Karrasch, P.A. Bullough, and R. Ghosh The 8.5 Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits EMBO J. 14 1995 631 638
6. S.J. Jamieson, P. Wang, P. Qian, J.Y. Kirkland, M.J. Conroy, C.N. Hunter, and P.A. Bullough Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 Å resolution EMBO J. 21 2002 3927 3935
7. S. Scheuring, J. Seguin, S. Marco, D. Levy, B. Robert, and J.-L. Rigaud Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM Proc. Natl Acad. Sci. USA 100 2003 1690 1693
8. D. Fotiadis, P. Qian, A. Philippsen, P.A. Bullough, A. Engel, and C.N. Hunter Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy J. Biol. Chem. 279 2004 2063 2068
9. C. Jungas, J.-L. Ranck, J.-L. Rigaud, P. Joliot, and A. Vermeglio Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides EMBO J. 18 1999 534 542
10. S. Scheuring, F. Francia, J. Busselez, B.A. Melandris, J.-L. Rigaud, and D. Levy Structural role of PufX in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides J. Biol. Chem. 279 2004 3620 3626
11. A.W. Roszak, T.D. Howard, J. Southall, A.T. Gardiner, C.J. Law, N.W. Isaac, and R.J. Cogdell Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris Science 302 2003 1969 1972
12. J.F. Miller, S.B. Hinchigeri, P.S. Parkes-Loach, P.M. Callahan, J.R. Sprinkle, J.R. Riccobono, and P.A. Loach Isolation and characterization of a subunit form of the light-harvesting complex of Rhodospirillum rubrum Biochemistry 26 1987 5055 5062
13. P.S. Parkes-Loach, J.R. Sprinkle, and P.A. Loach Reconstitution of the B873 light-harvesting complex of Rhodospirillum rubrum from the separately isolated α- and β-polypeptides and bacteriochlorophyll a Biochemistry 27 1988 2718 2727
14. M.C. Chang, P.M. Callahan, P.S. Parkes-Loach, T.M. Cotton, and P.A. Loach Spectroscopic characterization of the light-harvesting complex of Rhodospirillum rubrum and its structural subunit Biochemistry 29 1990 421 429
15. R.W. Visschers, M.C. Chang, F. van Mourik, P.S. Parkes-Loach, B.A. Heller, P.A. Loach, and R. van Grondelle Fluorescence polarization and low-temperature absorption spectroscopy of a subunit form of light-harvesting complex I from purple photosynthetic bacteria Biochemistry 30 1991 5734 5742
16. F. van Mourik, C.J.R. van der Oord, K.J. Visscher, P.S. Parkes-Loach, P.A. Parkes, R.W. Visschers, and R. van Grondelle Exciton interactions in the light-harvesting antenna of photosynthetic bacteria studied with triplet-singlet spectroscopy and singlet-triplet annihilation on the B820 subunit form of Rhodospirillum rubrum Biochim. Biophys. Acta 1059 1991 111 119
17. R.W. Visschers, R. van Grondelle, and B. Robert Resonance Raman spectroscopy of the B820 subunit of the core antenna from Rhodospirillum rubrum G9 Biochim. Biophys. Acta 1183 1993 369 373
18. A. Pandit, R.W. Visschers, I.H.M. van Stokkum, R. Kraayenhof, and R. van Grondelle Oligomerization of light-harvesting I antenna peptides of Rhodospirillum rubrum Biochemistry 40 2001 12913 12924
19. Z.-Y. Wang, Y. Muraoka, M. Nagao, M. Shibayama, M. Kobayashi, and T. Nozawa Determination of the B820 subunit size of a bacterial core light-harvesting complex by small-angle neutron scattering Biochemistry 42 2003 11555 11560
20. P.A. Loach, P.S. Parkes-Loach, C.M. Davis, and B.A. Heller Probing protein structural requirements for formation of the core light-harvesting complex of photosynthetic bacteria using hybrid reconstitution methodology Photosynth. Res. 40 1994 231 245
21. K.A. Meadows, K. Iida, K. Tsuda, P.A. Recchia, B.A. Heller, and B. Antonio Enzymatic and chemical cleavage of the core light-harvesting polypeptides of photosynthetic bacteria: determination of the minimal polypeptide size and structure required for subunit and light-harvesting complex formation Biochemistry 34 1995 1559 1574
22. C.M. Davis, P.S. Parkes-Loach, C.K. Cook, K.A. Meadows, M. Bandilla, H. Scheer, and P.A. Loach Comparison of the structural requirements for bacteriochlorophyll binding in the core light-harvesting complexes of Rhodospirillum rubrum and Rhodobacter sphaeroides using reconstitution methodology with bacteriochlorophyll analogs Biochemistry 35 1996 3072 3084
23. C.M. Davis, P.L. Bustamante, J.B. Todd, P.S. Parkes-Loach, P. McGlynn, J.D. Olsen, and L. McMaster Evaluation of structure-function relationships in the core light-harvesting complex of photosynthetic bacteria by reconstitution with mutant polypeptides Biochemistry 36 1997 3671 3679
24. K.A. Meadows, P.S. Parkes-Loach, J.W. Kehoe, and P.A. Loach Reconstitution of core light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides. 1. Minimal requirements for subunit formation Biochemistry 38 1998 3411 3417
25. V. Arluison, J. Seguin, J.-P. Le Caer, J.N. Sturgis, and B. Robert Hydrophobic pockets at the membrane interface: an original mechanism for membrane protein interactions Biochemistry 43 2004 1276 1282
26. J.N. Sturgis, J.D. Olsen, B. Robert, and C.N. Hunter Functions of conserved tryptophan residues of the core light-harvesting complex of Rhodobacter sphaeroides Biochemistry 36 1997 2772 2778
27. Z.-Y. Wang, Y. Muraoka, M. Shimonaga, M. Kobayashi, and T. Nozawa Selective detection and assignment of the solution NMR signals of bacteriochlorophyll a in a reconstituted subunit of a light-harvesting complex J. Am. Chem. Soc. 124 2002 1072 1078
28. J. Kikuchi, T. Asakura, P.A. Loach, P.S. Parkes-Loach, K. Shimada, and C.N. Hunter A light-harvesting antenna protein retains its folded conformation in the absence of protein-lipid and protein-pigment interactions Biopolymers 49 1999 361 372
29. M.J. Conroy, W.H.J. Westerhuis, P.S. Parkes-Loach, P.A. Loach, C.N. Hunter, and M.P. Williamson The solution structure of Rhodobacter sphaeroides LH1β reveals two helical domains separated by a more flexible region: structural consequences for the LH1 complex J. Mol. Biol. 298 2000 83 94
30. P.L. Sorgen, S.M. Cahill, R.D. Krueger-Koplin, S.T. Krueger-Koplin, C.C. Schenck, and M.E. Girvin Structure of the Rhodobacter sphaeroides light-harvesting 1 β subunit in detergent micelles Biochemistry 41 2002 31 41
31. L. Germeroth, F. Lottspeich, B. Robert, and H. Michel Unexpected similarities of the B800-850 light-harvesting complex from Rhodospirillum molischianum to the B870 light-harvesting complexes from other purple photosynthetic bacteria Biochemistry 32 1993 5615 5621
32. J.B. Todd, P.A. Parks-Loach, J.F. Leykam, and P.A. Loach In vitro reconstitution of the core and peripheral light-harvesting complexes of Rhodospirillum molischianum from separately isolated components Biochemistry 37 1998 17458 17468
33. P.S. Parkes-Loach, A.P. Majeed, C.J. Law, and P.A. Loach Interactions stabilizing the structure of the core light-harvesting complex (LH1) of photosynthetic bacteria and its subunit (B820) Biochemistry 43 2004 7003 7016
34. o ATP synthase Biochemistry 37 1998 8817 8824
35. U. Matthey, G. Kaim, D. Braun, K. Wuthrich, and P. Dimroth NMR studies of subunit c of the ATP synthase from Propionigenium modestum in dodecylsulphate micelles Eur. J. Biochem. 261 1999 459 467
36. R.D. Krueger-Koplin, P.L. Sorgen, S.T. Krueger-Koplin, I.O. Rivera-Torres, S.M. Cahill, and D.B. Hicks An evaluation of detergents for NMR structural studies of membrane proteins J. Biomol. NMR 17 2004 43 57
37. 1H NMR experiments show that the 23-residue magainin antibiotic peptide is an α-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution J. Biomol. NMR 9 1997 127 135
38. A. Arora, F. Abildgaard, J.H. Bushweller, and L.K. Tamm Structure of outer membrane protein A transmembrane domain by NMR spectroscopy Nature Struct. Biol. 8 2001 334 338
39. R. Ghosh, H. Hauser, and R. Bachofen Reversible dissociation of the B873 light-harvesting complex from Rhodospirillum rubrum G9+ Biochemistry 27 1988 1004 1014
40. W.P. Russ, and D.M. Engelman The GxxxG motif: a framework for transmembrane helix-helix association J. Mol. Biol. 296 2000 911 919
41. A. Senes, M. Gerstein, and D.M. Engelman Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with β-branched residues at neighboring positions J. Mol. Biol. 296 2000 921 936
42. G. Kleiger, R. Grothe, P. Mallick, and D. Eisenberg GXXXG and AXXXA common α-helical interaction motifs in proteins, particularly in extremophiles Biochemistry 41 2002 5990 5997
43. R.A. Melnyk, S. Kim, A.R. Currant, D.M. Engelman, J.U. Bowie, and C.M. Deber The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication J. Biol. Chem. 279 2004 16591 16597
44. K.R. MacKenzie, J.H. Prestegard, and D.M. Engelman A transmembrane helix dimer: structure and implications Science 276 1997 131 133
45. J.W. Kehoe, K.A. Meadows, P.S. Parkes-Loach, and P.A. Loach Reconstitution of core light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides. 2. Determination of structural features that stabilize complex formation and their implications for the structure of the subunit complex Biochemistry 38 1998 3418 3428
46. H. Zuber, and R.J. Cogdell Structure and organization of purple bacterial antenna complexes R.E. Blankenship M.T. Madigan C.D. Bauer Anoxygenic Photosynthetic Bacteria 1995 Kluwer Academic Publishers Dordrecht, The Netherlands 315 348
47. α-H⋯O hydrogen bonds and van der Waals interactions J. Mol. Biol. 323 2002 69 76
48. V. Kairys, M.K. Gilson, and B. Luy Structural model for an AXXXG-mediated dimer of surfactant-associated protein C Eur. J. Biochem. 271 2004 2086 2092
49. B. Dörge, G. Klug, N. Gad'on, S.N. Cohen, and G. Drews Effects on the formation of antenna complex B870 of Rhodobacter capsulatus by exchange of charged amino acids in the N-terminal domains of the α and β pigment-binding proteins Biochemistry 29 1990 7754 7758
50. H. Stiehle, N. Cortez, G. Klug, and G. Drews Negatively charged N terminus in the α polypeptide inhibits formation of light-harvesting complex I in Rhodobacter capsulatus J. Bacteriol. 172 1990 7131 7137
51. J.G. Ormerod, K.S. Ormerod, and H. Gest Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism Arch. Biochem. Biophys. 94 1961 449 463
52. Y.-H. Chen, J.T. Yang, and M. Martinez Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion Biochemistry 11 1972 4120 4131
53. A.L. Davis, J. Keeler, E.D. Laue, and D. Moskau Experiments for recording pure-absorption heteronuclear correlation spectra using pulsed field gradients J. Magn. Reson. 98 1992 207 216
54. 2O saturation J. Magn. Reson. ser. A 109 1994 129 133
55. J. Stonehouse, R.T. Clowes, G.L. Shaw, J. Keeler, and E.D. Laue Minimisation of sensitivity losses due to the use of gradient pulses in triple-resonance NMR of protein J. Biomol. NMR 5 1995 226 232
56. A. Bax, and S.S. Pochapsky Optimized recording of heteronuclear multidimensional NMR spectra using pulsed field gradients J. Magn. Reson. 99 1992 638 643
57. S. Grzesiek, and A. Bax An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins J. Magn. Reson. 99 1992 201 207
58. D.R. Muhandiram, and L.E. Kay Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity J. Magn. Reson. ser. B 103 1994 203 216
59. A.C. Wang, P.J. Lodi, J. Qin, G.W. Vuister, A.M. Gronenborn, and G.M. Clore An efficient triple-resonance experiment for proton-directed sequential backbone assignment of medium-sized proteins J. Magn. Reson. ser. B 105 1994 196 198
60. 15N-enriched proteins J. Biomol. NMR 3 1993 185 204
61. 13C magnetization J. Magn. Reson. ser. B 101 1993 114 119
62. T.M. Logan, E.T. Olejniczak, R.X. Xu, and S.W. Fesik A general method for assigning NMR spectra of denatured proteins using 3D HC(CO)NH-TOCSY triple resonance experiments J. Biomol. NMR 3 1993 225 231
63. 2O samples of proteins J. Magn. Reson. ser. B 101 1993 333 337
64. 15N-enriched proteins J. Am. Chem. Soc. 115 1993 7772 7777
65. 15N chemical shift referencing in biomolecular NMR J. Biomol. NMR 6 1995 135 140
66. F. Delaglio, S. Grzesiek, G. Zhu, G.W. Vuister, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
67. B.A. Johnson, and R.A. Blevins NMRView: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
68. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
69. R.A. Laskowski, J.A.C. Rullmann, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and ROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486
70. R. Koradi, M. Billeter, and K. Wüthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55