The importance of protein-protein interactions for optimising oxygen activity in photosystem II: Reconstitution with a recombinant thioredoxin-manganese stabilising protein

Photosynthesis Research

Volumn 92, Issue 3, 2007, Pages 305-314

  Williamson, A K ^a   Liggins, J R ^a   Hillier, W ^a   Wydrzynski, T ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Calcium binding; Chimeric protein; Conformational flexibility; Differential scanning calorimetry; Manganese stabilising protein; Oxygen evolution

Indexed keywords

BACTERIAL PROTEIN; OXYGEN; PHOTOSYSTEM II MANGANESE STABILIZING PROTEIN; PHOTOSYSTEM II MANGANESE-STABILIZING PROTEIN; RECOMBINANT PROTEIN; THIOREDOXIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CYANOBACTERIUM; ESCHERICHIA COLI; METABOLISM; MOLECULAR GENETICS; PHOTOSYSTEM II; PROTEIN BINDING; TEMPERATURE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYANOBACTERIA; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN BINDING; RECOMBINANT PROTEINS; TEMPERATURE; THIOREDOXIN;

EMBRYOPHYTA; ESCHERICHIA COLI; SPINACIA OLERACEA; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 34547851703     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-007-9165-1     Document Type: Article

References (63)

1. Ahmed A, Tajmirriahi HA, Carpentier R (1995) A quantitative secondary structure-analysis of the 33-kDa extrinsic polypeptide of photosystem-II by FTIR spectroscopy. Febs Lett 363:65-68
2. Al-Khaldi SF, Coker J, Shen JR, Burnap RL (2000) Characterization of site-directed mutants in manganese-stabilizing protein (msp) of synechocystis sp pcc6803 unable to grow photoautotrophically in the absence of cytochrome c-550. Plant Mol Biol 43:33-41
3. Aslanidis C, Dejong PJ (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 18:6069-6074
4. Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved, oxygen-evolving photosystem-II preparation from spinach thylakoid membranes-electron paramagnetic resonance and electron transport properties. Febs Lett 134:231-234
5. Bricker TM (1992) Oxygen evolution in the absence of the 33-kilodalton manganese-stabilizing protein. Biochemistry 31:4623-4628
6. Bricker TM, Burnap RL (2005) The extrinsic proteins of photosystem II. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: plastoquinone oxidoreductase, vol 22. Springer, pp 95-120
7. Campbell KA, Gregor W, Pham DP, Peloquin JM, Debus RJ, Britt RD (1998) The 23 and 17 kDa extrinsic proteins of photosystem II modulate the magnetic properties of the S1-state manganese cluster. Biochemistry 37:5039-5045
8. De Las Rivas J, Barber J (2004) Analysis of the structure of the Psbo protein and its implications. Photosynth Res 81:329-343
9. Eaton-Rye J J, Putnam-Evans E (2005) The cp47 and cp43 core antenna components. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22, Springer, pp 45-70
10. Enami I, Kamo M, Ohta H, Takahashi S, Miura T, Kusayanagi M, Tanabe S, Kamei A, Motoki A, Hirano M, Tomo T, Satoh K (1998) Intramolecular cross-linking of the extrinsic 33-kDa protein leads to loss of oxygen evolution but not its ability of binding to photosystem II and stabilization of the manganese cluster. J Biol Chem 273:4629-4634
11. Enami I, Yoshihara S, Tohri A, Okumura A, Ohta H, Shen JR (2000) Cross-reconstitution of various extrinsic proteins and photosystem II complexes from cyanobacteria, red algae and higher plants. Plant Cell Physiol 41:1354-1364
12. Ford RC, Evans MCW (1983) Isolation of a photosystem II preparation from higher-plants with highly enriched oxygen evolution activity. Febs Lett 160:159-164
13. Frankel LK, Cruz JA, Bricker TM (1999) Carboxylate groups on the manganese-stabilizing protein are required for its efficient binding to photosystem II. Biochemistry 38:14271-14278
14. Ghanotakis DF, Babcock GT, Yocum CF (1984a) Calcium reconstitutes high-rates of oxygen evolution in polypeptide depleted photosystem-II preparations. Febs Lett 167:127-130
15. 2+ on the oxidizing side of photosystem-II. Febs Lett 170:169-173
16. Haun RS, Serventi IM, Moss J (1992) Rapid, reliable ligation-independent cloning of PCR products using modified plasmid vectors. Biotechniques 13:515-518
17. Henmi T, Miyao M, Yamamoto Y (2004) Release and reactive-oxygen-mediated damage of the oxygen-evolving complex subunits of PSII during photoinhibition. Plant Cell Physiol 45:243-250
18. Henmi T, Yamasaki H, Sakuma S, Tomokawa Y, Tamura N, Shen MR, Yamamoto Y (2003) Dynamic interaction between the d1 protein, CP43 and OEC33 at the lumenal side of photosystem II in spinach chloroplasts: Evidence from light induced cross-linking of the proteins in the donor-side photoinhibition. Plant Cell Physiol 44:451-456
19. Heredia P, De Las Rivas J (2003) Calcium-dependent conformational change and thermal stability of the isolated PsbO protein detected by FTIR spectroscopy. Biochemistry 42:11831-11838
20. Hillier W, Hendry G, Burnap RL, Wydrzynski T (2001) Substrate water exchange in photosystem II depends on the peripheral proteins. J Biol Chem 276:46917-46924
21. Hong SK, Pawlikowski SA, Vander Meulen KA, Yocum CF (2001) The oxidation state of the photosystem II manganese cluster influences the structure of manganese stabilizing protein. Biochim Biophys Acta 1504:262-274
22. Hutchison RS, Betts SD, Yocum CF, Barry BA (1998) Conformational changes in the extrinsic manganese stabilizing protein can occur upon binding to the photosystem II reaction center: An isotope editing and FTIR study. Biochemistry 37:5643-5653
23. Ishikita H, Saenger W, Loll B, Biesiadka J, Knapp EW (2006) Energetics of a possible proton exit pathway for water oxidation in photosystem II. Biochemistry 45:2063-2071
24. Kruk J, Burda K, Jemiola-Rzeminska M, Strzalka K (2003) The 33 kDa protein of photosystem II is a low-affinity calcium- and lanthanide-binding protein. Biochemistry 42:14862-14867
25. Kuwabara T, Miyao M, Murata T, Murata N (1985) The function of 33-kDa protein in the photosynthetic oxygen-evolution system studied by reconstitution experiments. Biochim Biophys Acta 806:283-289
26. Ladbury JE, Wynn R, Hellinga HW, Sturtevant JM (1993) Stability of oxidized Escherichia-coli thioredoxin and its dependence on protonation of the aspartic-acid residue in the 26 position. Biochemistry 32:7526-7530
27. Lavallie ER, Mccoy JM (1995) Gene fusion expression systems Escherichia-coli. Curr Opin Biotech 6:501-506
28. 2+ binding properties of wild type and heterologously expressed PsbO protein from cyanobacterial photosystem II. Biochemistry 44:4691-4698
29. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005b) Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of photosystem II. Nature 438:1040-1044
30. Miura T, Shen JR, Takahashi S, Kamo M, Nakamura E, Ohta H, Kamei A, Inoue Y, Domae N, Takio R, Nakazato K, Inoue Y, Enami I (1997) Identification of domains on the extrinsic 33-kDa protein possibly involved in electrostatic interaction with photosystem II complex by means of chemical modification. J Biol Chem 272:3788-3798
31. Miyao M, Murata N (1984a) Calcium-ions can be substituted for the 24-kda polypeptide in photosynthetic oxygen evolution. Febs Lett 168:118-120
32. Miyao M, Murata N (1984b) Effect of urea on photosystem-II particles - evidence for an essential role of the 33 kDa polypeptide in photosynthetic oxygen evolution. Biochim Biophys Acta 765:253-257
33. Miyao M, Murata N (1984c) Role of the 33-kDa polypeptide in preserving Mn in the photosynthetic oxygen-evolution system and its replacement by chloride-ions. Febs Lett 170:350-354
34. Motoki A, Usui M, Shimazu T, Hirano M, Katoh S (2002) A domain of the manganese-stabilizing protein from synechococcus elongatus involved in functional binding to photosystem II. J Biol Chem 277:14747-14756
35. Murata N, Miyao M, Omata T, Matsunami H, Kuwabara T (1984) Stoichiometry of components in the photosynthetic oxygen evolution system of photosystem-II particles prepared with triton X-100 from spinach-chloroplasts. Biochim Biophys Acta 765:363-369
36. Murray JW, Barber J (2006) Identification of a calcium-binding site in the psbo protein of photosystem II. Biochemistry 45:4128-4130
37. Nixon PJS, Sarcina M, Diner BA (2005) The D1 and D2 core proteins. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: plastoquinone oxidoreductase, vol 22. Springer, pp 71-94
38. Nowaczyk M, Berghaus C, Stoll R, Rogner M (2004) Preliminary structural characterisation of the 33 kDa protein (PsbO) in solution studied by site-directed mutagenesis and NMR spectroscopy. Phys Chem Chem Phys 6:4878-4881
39. 2-extracted PS-II particles. Febs Lett 166:381-384
40. Philbrick JB, Diner BA, Zilinskas BA (1991) Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing polypeptide of photosystem-II. J Biol Chem 266:13370-13376
41. Popelkova H, Im MM, D'Auria J, Betts SD, Lydakis-Simantiris N, Yocum CF (2002a) N-terminus of the photosystem II manganese stabilizing protein: effects of sequence elongation and truncation. Biochemistry 41:2702-2711
42. Popelkova H, Im MM, Yocum CF (2002b) N-terminal truncations of manganese stabilizing protein identify two amino acid sequences required for binding of the eukaryotic protein to photosystem II and reveal the absence of one binding-related sequence in cyanobacteria. Biochemistry 41:10038-10045
43. Popelkova H, Im MM, Yocum CF (2003a) Binding of manganese stabilizing protein to photosystem II: identification of essential N-terminal threonine residues and domains that prevent nonspecific binding. Biochemistry 42:6193-6200
44. Popelkova H, Wyman A, Yocum C (2003b) Amino acid sequences and solution structures of manganese stabilizing protein that affect reconstitution of photosystem II activity. Photosynth Res 77:21-34
45. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents-verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim Biophys Acta 975:384-394
46. 4 cluster in site-directed mutants impaired in the binding of the manganese-stabilizing protein. Biochemistry 36:15244-15252
47. Sachs RK, Halverson KM, Barry BA (2003) Specific isotopic labeling and photooxidation-linked structural changes in the manganese-stabilizing subunit of photosystem II. J Biol Chem 278:44222-44229
48. Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta Bioenergetics 1277:35-60
49. Shutova T, Irrgang KD, Klimov VV, Renger G (2000) Is the manganese stabilizing 33 kDa protein of photosystem II attaining a 'natively unfolded' or 'molten globule' structure in solution? Febs Lett 467:137-140
50. Shutova T, Irrgang KD, Shubin V, Klimov VV, Renger G (1997) Analysis of pH induced structural changes of the isolated extrinsic 33 kilodalton protein of photosystem II. Biochemistry 36:6350-6358
51. Shutova T, Nikitina J, Deikus G, Andersson B, Klimov V, Samuelsson G (2005) Structural dynamics of the manganese-stabilizing protein-effect of pH, calcium, and manganese. Biochemistry 44:15182-15192
52. Shutova T, Villarejo A, Zietz B, Klimov V, Gillbro T, Samuelsson G, Renger G (2003) Comparative studies on the properties of the extrinsic manganese-stabilizing protein from higher plants and of a synthetic peptide of its C-terminus. Biochim Biophys Acta Bioenergetics 1604:95-104
53. Sonoyama M, Motoki A, Okamoto G, Hirano M, Ishida H, Katoh S (1996) Secondary structure and thermostability of the photosystem II manganese-stabilizing protein of the thermophilic cyanobacterium synechococcus elongatus. Biochim Biophys Acta 1297:167-170
54. Sturtevant JM (1987) Biochemical applications of differential scanning calorimetry. Annu Rev Phys Chem 38:463-488
55. Svensson B, Tiede DM, Nelson DR, Barry BA (2004) Structural studies of the manganese stabilizing subunit in photosystem II. Biophys J 86:1807-1812
56. Tohri A, Suzuki T, Okuyama S, Kamino K, Motoki A, Hirano M, Ohta H, Shen JR, Yamamoto Y, Enami I (2002) Comparison of the structure of the extrinsic 33 kDa protein from different organisms. Plant Cell Physiol 43:429-439
57. Wydrzynski T, Hillier W, Messinger J (1996) On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism. Physiol Plantarum 96:342-350
58. Wydrzynski T, Satoh K (eds) (2006) Photosystem II, the light driven water: plastoquinone oxidoreductase. vol 22, Advances in photosynthesis and respiration, Springer
59. Wyman AJ, Yocum CF (2005) Assembly and function of the photosystem II manganese stabilizing protein: Lessons from its natively unfolded behavior. Photosynth Res 84:283-288
60. Xu Q, Nelson J, Bricker TM (1994) Secondary structure of the 33 kDa, extrinsic protein of photosystem-II - a far-UV circular-dichroism study. Biochim Biophys Acta 1188:427-431
61. Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121-128
62. Yamamoto Y, Ishikawa Y, Nakatani E, Yamada M, Zhang HM, Wydrzynski T (1998) Role of an extrinsic 33 kilodalton protein of photosystem II in the turnover of the reaction center-binding protein D1 during photoinhibition. Biochemistry 37:1565-1574
63. Zamyatnin (1971) Volume of protein in solutions. Biophys J 16:169-171