Design of a minimal polypeptide unit for bacteriochlorophyll binding and self-assembly based on photosynthetic bacterial light-harvesting proteins

Biochemistry

Volumn 45, Issue 7, 2006, Pages 2103-2113

  Noy, Dror ^a,b   Dutton, P Leslie ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; CRYSTAL STRUCTURE; ENTHALPY; OLIGOMERS; PROTEINS; SELF ASSEMBLY;

BACTERIAL LH PROTEINS; BACTERIOCHLOROPHYLL BINDING; BACTERIOCHLOROPHYLLS; LIGHT-HARVESTING PROTEINS;

POLYPEPTIDES;

AMINO ACID; APOLIPOPROTEIN B; BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL; GLUCOSIDE; OCTYL BETA GLUCOSIDE; OLIGOMER; POLYPEPTIDE; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COOLING; CRYSTAL STRUCTURE; DNA MODIFICATION; ENTHALPY; ENTROPY; IN VITRO STUDY; IN VIVO STUDY; LIGHT HARVESTING SYSTEM; MICELLE; NONHUMAN; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEOBACTERIA; RHODOBACTER SPHAEROIDES; RHODOSPIRILLUM; RHODOSPIRILLUM MOLISCHIANUM; RHODOSPIRILLUM RUBRUM; SPECTRUM;

AMINO ACID SEQUENCE; BACTERIOCHLOROPHYLLS; CENTRIFUGATION; CIRCULAR DICHROISM; LIGHT-HARVESTING PROTEIN COMPLEXES; MOLECULAR SEQUENCE DATA; PHOTOSYSTEM I PROTEIN COMPLEX; PROTEIN ENGINEERING; SEQUENCE ALIGNMENT; SPECTROPHOTOMETRY; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); PHAEOSPIRILLUM MOLISCHIANUM; PHOTOBACTERIA; PROTEOBACTERIA; RHODOBACTER SPHAEROIDES; RHODOSPIRILLUM; RHODOSPIRILLUM RUBRUM;

EID: 33144468377     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052175x     Document Type: Article

References (60)

1. Robertson, D. E., Fand, R. S., Moser, C. C., Urbauer, J. L., Mulholland, S. E., Pidikiti, R., Lear, J. D., Wand, A. J., Degrade, W. F., and Dutton, P. L. (1994) Design and synthesis of multi-heme proteins, Nature 368, 425-431.
2. Chen, X. X., Discher, B. M., Pilloud, D. L., Gibney, B. R., Moser, C. C., and Dutton, P. L. (2002) De novo design of a cytochrome b maquette for electron transfer and coupled reactions on electrodes, J. Phys. Chem. B 106, 617-624.
3. Discher, B. M., Noy, D., Strzalka, J., Ye, S., Moser, C. C., Lear, J. D., Blasie, J. K., and Dutton, P. L. (2005) Design of amphiphilic protein maquettes: controlling assembly, membrane insertion, and cofactor interactions, Biochemistry 44, 12329-12343.
4. Gibney, B. R., Rabanal, F., Reddy, K. S., and Dutton, P. L. (1998) Effect of four helix bundle topology on heme binding and redox properties, Biochemistry 37, 4635-4643.
5. Grosset, A. M., Gibney, B. R., Rabanal, F., Moser, C. C., and Dutton, P. L. (2001) Proof of principle in a de novo designed protein maquette: An allosterically regulated, charge-activated conformational switch in a tetra-alpha-helix bundle, Biochemistry 40, 5474-5487.
6. Noy, D., Discher, B. M., Rubtsov, I. V., Hochstrasser, R. M., and Dutton, P. L. (2005) Design of amphiphilic protein maquettes: Enhancing maquette functionality through binding of extremely hydrophobic cofactors to lipophilic domains, Biochemistry 44, 12344-12354.
7. Sharp, R. E., Moser, C. C., Rabanal, F., and Dutton, P. L. (1998) Design, synthesis, and characterization of a photoactivatable flavocytochrome molecular maquette, Proc. Natl. Acad. Sci. U.S.A. 95, 10465-10470.
8. Sharp, R. E., Diers, J. R., Bocian, D. F., and Dutton, P. L. (1998) Differential binding of iron(III) and zinc(II) protoporphyrin IX to synthetic four-helix bundles, J. Am. Chem. Soc. 120, 7103-7104.
9. Shifman, J. M., Moser, C. C., Kalsbeck, W. A., Bocian, D. F., and Dutton, P. L. (1998) Functionalized de novo designed proteins: Mechanism of proton coupling to oxidation/reduction in heme protein maquettes, Biochemistry 37, 16815-16827.
10. Shifman, J. M., Gibney, B. R., Sharp, R. E., and Dutton, P. L. (2000) Heme redox potential control in de novo designed four-alpha-helix bundle proteins, Biochemistry 39, 14813-14821.
11. Tommos, C., Skalicky, J. J., Pilloud, D. L., Wand, A. J., and Dutton, P. L. (1999) De novo proteins as models of radical enzymes, Biochemistry 38, 9495-9507.
12. Noy, D., Moser, C. C., and Dutton, P. L. (2005) Design and engineering of photosynthetic light-harvesting and electron-transfer using length, time, and energy scales, Biochim. Biophys. Acta (in press).
13. Moser, C. C., Page, C. C., Cogdell, R. J., Barber, J., Wraight, C. A., and Dutton, P. L. (2003) Length, time, and energy scales of photosystems, Adv. Protein Chem. 63, 71-109.
14. Chamberlain, A. K., Faham, S., Yohannan, S., and Bowie, J. U. (2003) Construction of helix-bundle membrane proteins, Adv. Protein Chem. 63, 19-46.
15. Barker, P. D. (2003) Designing redox metalloproteins from bottom-up and top-down perspectives, Curr. Opin. Struct. Biol. 13, 490-499.
16. Prince, S. M., Papiz, M. Z., Freer, A. A., McDermott, G., Hawthornthwaite-Lawless, A. M., Cogdell, R. J., and Isaacs, N. W. (1997) Apoprotein structure in the LH2 complex from Rhodopseudomonas acidophila strain 10050: Modular assembly and protein pigment interactions, J. Mol. Biol. 268, 412-423.
17. Koepke, J., Hu, X. C., Muenke, C., Schulten, K., and Michel, H. (1996) The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum, Structure 4, 581-597.
18. Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., and Krauss, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution, Nature 411, 909-917.
19. McLuskey, K., Prince, S. M., Cogdell, R. J., and Isaacs, N. W. (2001) The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050, Biochemistry 40, 8783-8789.
20. Kamiya, N., and Shen, J. R. (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-angstrom resolution, Proc. Natl. Acad. Sci. U.S.A. 100, 98-103.
21. Liu, Z. F., Yan, H. C., Wang, K. B., Kuang, T. Y., Zhang, J. P., Gui, L. L., An, X. M., and Chang, W. R. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 angstrom resolution, Nature 428, 287-292.
22. McDermott, G., Prince, S. M., Freer, A. A., Hawthornthwaite-Lawless, A. M., Papiz, M. Z., Cogdell, R. J., and Isaacs, N. W. (1995) Crystal-structure of an integral membrane light-harvesting complex from photosynthetic bacteria, Nature 374, 517-521.
23. Bibby, T. S., Nield, J., Chen, M., Larkum, A. W., and Barber, J. (2003) Structure of a photosystem II supercomplex isolated from Prochloron didemni retaining its chlorophyll a/b light-harvesting system, Proc. Natl. Acad. Sci. U.S.A. 100, 9050-9054.
24. Ben-Shem, A., Frolow, F., and Nelson, N. (2003) Crystal structure of plant photosystem I, Nature 426, 630-635.
25. Papiz, M. Z., Prince, S. M., Howard, T., Cogdell, R. J., and Isaacs, N. W. (2003) The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100 K: New structural features and functionally relevant motions, J. Mol. Biol. 326, 1523-1538.
26. Roszak, A. W., Howard, T. D., Southall, J., Gardiner, A. T., Law, C. J., Isaacs, N. W., and Cogdell, R. J. (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris, Science 302, 1969-1972.
27. Camara-Artigas, A., and Allen, J. P. (2004) Comparative analyses of three-dimensional models of bacterial reaction centers, Photosynth. Res. 81, 227-237.
28. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution, Nature 318, 618-624.
29. Parkes-Loach, P. S., Sprinkle, J. R., and Loach, P. A. (1988) Reconstitution of the B873 light-harvesting complex of Rhodospirillum rubrum from the separately isolated alpha-polypeptide and beta-polypeptide and bacteriochlorophyll-A, Biochemistry 27, 2718-2727.
30. Kehoe, J. W., Meadows, K. A., Parkes-Loach, P. S., and Loach, P. A. (1998) 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 37, 3418-3428.
31. Meadows, K. A., Iida, K., Tsuda, K., Recchia, P. A., Heller, B. A., Antonio, B., Nango, M., and Loach, P. A. (1995) 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, 1559-1574.
32. Meadows, K. A., Parkes-Loach, P. S., Kehoe, J. W., and Loach, P. A. (1998) Reconstitution of core light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides. 1. Minimal requirements for subunit formation, Biochemistry 37, 3411-3417.
33. Parkes-Loach, P. S., Michalski, T. J., Bass, W. J., Smith, U., and Loach, P. A. (1990) Probing the bacteriochlorophyll binding-site by reconstitution of the light-harvesting complex of Rhodospirillum rubrum with bacteriochlorophyll-a analogues, Biochemistry 29, 2951-2960.
34. Todd, J. B., Recchia, P. A., Parkes-Loach, P. S., Olsen, J. D., Fowler, G. J. S., McGlynn, P., Hunter, C. N., and Loach, P. A. (1999) Minimal requirements for in vitro reconstitution of the structural subunit of light-harvesting complexes of photosynthetic bacteria, Photosynth. Res. 62, 85-98.
35. Kwa, L. G., Garcia-Martin, A., Vegh, A. P., Strohmann, B., Robert, B., and Braun, P. (2004) Hydrogen bonding in a model bacteriochlorophyll-binding site drives assembly of light harvesting complex, J. Biol. Chem. 279, 15067-15075.
36. Braun, P., Olsen, J. D., Strohmann, B., Hunter, C. N., and Scheer, H. (2002) Assembly of light-harvesting bacteriochlorophyll in a model transmembrane helix in its natural environment, J. Mol. Biol. 318, 1085-1095.
37. Fowler, G. J. S., Sockalingum, G. D., Robert, B., and Hunter, C. N. (1994) Blue shifts in bacteriochlorophyll absorbency correlate with changed hydrogen-bonding patterns in light-harvesting 2 mutants of Rhodobacter sphaeroides with alterations at alpha-Tyr-44 and alpha-Tyr-45, Biochem. J. 299, 695-700.
38. Fowler, G. J. S., Hess, S., Pullerits, T., Sundstrom, V., and Hunter, C. N. (1997) The role of beta Arg(-10) in the B800 bacteriochlorophyll and carotenoid pigment environment within the light-harvesting LH2 complex of Rhodobacter sphaeroides, Biochemistry 36, 11282-11291.
39. Olsen, J. D., Sturgis, J. N., Westerhuis, W. H. J., Fowler, G. J. S., Hunter, C. N., and Robert, B. (1997) Site-directed modification of the ligands to the bacteriochlorophylls of the light-harvesting LH1 and LH2 complexes of Rhodobacter sphaeroides, Biochemistry 36, 12625-12632.
40. Sturgis, J. N., Olsen, J. D., Robert, B., and Hunter, C. N. (1997) Functions of conserved tryptophan residues of the core light-harvesting complex of Rhodobacter sphaeroides, Biochemistry 36, 2772-2778.
41. Loach, P. A., and Parkes-Loach, P. S. (1995) Structure-function relationships in core light-harvesting complexes (LHI) as determined by charterization of the structural subunit and by reconstitution experiments, in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 437-471, Kluwer Academic Publishers, Dordrecht.
42. Visschers, R. W., Chang, M. C., Vanmourik, F., Parkesloach, P. S., Heller, B. A., Loach, P. A., and Vangrondelle, R. (1991) Fluorescence polarization and low-temperature absorption-spectroscopy of a subunit form of light-harvesting complex-I from purple photosynthetic bacteria, Biochemistry 30, 5734-5742.
43. Chang, M. C., Callahan, P. M., Parkesloach, P. S., Cotton, T. M., and Loach, P. A. (1990) Spectroscopic characterization of the light-harvesting complex of Rhodospirillum rubrum and its structural subunit, Biochemistry 29, 421-429.
44. Wang, Z. Y., Muraoka, Y., Nagao, M., Shibayama, M., Kobayashi, M., and Nozawa, T. (2003) Determination of the B820 subunit size of a bacterial core light-harvesting complex by small-angle neutron scattering, Biochemistry 42, 11555 -11560.
45. Todd, J. B., Parkes-Loach, P. S., Leykam, J. F., and Loach, P. A. (1998) In vitro reconstitution of the core and peripheral light-harvesting complexes of Rhodospirillum molischianum from separately isolated components, Biochemistry 37, 17458-17468.
46. Novoderezhkin, V., Monshouwer, R., and van Grondelle, R. (1999) Exciton (de)localization in the LH2 antenna of Rhodobacter sphaeroides as revealed by relative difference absorption measurements of the LH2 antenna and the B820 subunit, J. Phys. Chem. B 103, 10540-10548.
47. Koolhaas, M. H. C., vanderZwan, G., vanMourik, F., and vanGrondelle, R. (1997) Spectroscopy and structure of bacteriochlorophyll dimers. 1. Structural consequences of nonconservative circular dichroism spectra, Biophys. J. 72, 1828-1841.
48. Kashiwada, A., Watanabe, H., Tanaka, T., and Nango, M. (2000) Molecular assembly of zinc bachteriochlorophyll a by synthetic hydrophobic 1 alpha-helix polypeptides, Chem. Lett., 24-25.
49. Nagata, M., Nango, M., Kashiwada, A., Yamada, S., Ito, S., Sawa, N., Ogawa, M., Iida, K., Kurono, Y., and Ohtsuka, T. (2003) Construction of photosynthetic antenna complex using light-harvesting polypeptide-alpha from photosynthetic bacteria, R. rubrum with zinc substituted bacteriochlorophyll alpha, Chem. Lett. 32, 216-217.
50. Nango, M., Kashiwada, A., Watanabe, H., Yamada, S., Yamada, T., Ogawa, M., Tanaka, T., and Iida, K. (2002) Molecular assembly of bachteriochlorophyll a using light-harvesting model 1 alpha-helix polypeptides and 2 alpha-helix polypeptide with disulfide-linkage, Chem. Lett., 312-313.
51. Kashiwada, A., Takeuchi, Y., Watanabe, H., Mizuno, T., Yasue, H., Kitagawa, K., Iida, K., Wang, Z. Y., Nozawa, T., Kawai, H., Nagamura, T., Kurono, Y., and Nango, M. (2000) Molecular assembly of covalently-linked mesoporphyrin dimers with light-harvesting polypeptides, Tetrahedron Lett. 41, 2115-2119.
52. Kashiwada, A., Watanabe, H., Mizuno, T., Iida, K., Miyatake, T., Tamiaki, H., Kobayashi, M., and Nango, M. (2000) Structural requirements of zinc porphyrin derivatives on the complex-forming with light-harvesting polypeptides, Chem. Lett., 158-159.
53. Dewa, T., Yamada, T., Ogawa, M., Sugimoto, M., Mizuno, T., Yoshida, K., Nakao, Y., Kondo, M., Iida, K., Yamashita, K., Tanaka, T., and Nango, M. (2005) Design and expression of cysteine-bearing hydrophobic polypeptides and their self-assembling properties with bacteriochlorophyll a derivatives as a mimic of bacterial photosynthetic antenna complexes. Effect of steric confinement and orientation of the polypeptides on the pigment/polypeptide assembly process, Biochemistry 44, 5129-5139.
54. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics, J. Mol. Graphics 14, 33-38.
55. Georgakopoulou, S., Frese, R. N., Johnson, E., Koolhaas, C., Cogdell, R. J., van Grondelle, R., and van der Zwan, G. (2002) Absorption and CD spectroscopy and modeling of various LH2 complexes from purple bacteria, Biophys. J. 82, 2184-2197.
56. Scherz, A., and Rosenbach-Belkin, V. (1989) Comparative-study of optical-absorption and circular-dichroism of bacteriochlorophyll oligomers in Triton X-100, the antenna pigment B850, and the primary donor P-860 of photosynthetic bacteria indicates that all are similar dimers of bacteriochlorophyll-A, Proc. Natl. Acad. Sci. U.S.A. 86, 1505-1509.
57. Pandit, A., Visschers, R. W., van Stokkum, I. H. M., Kraayenhof, R., and van Grondelle, R. (2001) Oligomerization of light-harvesting I antenna peptides of Rhodospirillum rubrum, Biochemistry 40, 12913-12924.
58. Davis, C. M., ParkesLoach, P. S., Cook, C. K., Meadows, K. A., Bandilla, M., Scheer, H., and Loach, P. A. (1996) 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, 3072-3084.
59. Sturgis, J. N., and Robert, B. (1994) Thermodynamics of membrane polypeptide oligomerization in light-harvesting complexes and associated structural-changes, J. Mol. Biol. 238, 445-454.
60. Parkes-Loach, P. S., Majeed, A. P., Law, C. J., and Loach, P. A. (2004) Interactions stabilizing the structure of the core light-harvesting complex (LH1) of photosynthetic bacteria and its subunit (B820), Biochemistry 43, 7003-7016.