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Circularly Polarized Luminescence (CPL) of Proteins and Protein Complexes

  • Eugene Gussakovsky
Part of the Reviews in Fluorescence 2008 book series (RFLU, volume 2008)

Abstract

The review considers general theory of circularly polarized luminescence (CPL), instrumentation employed for its accurate measurement including artifacts, calibration, principle parts, and its application to proteins and protein complexes. Circularly polarized intrinsic fluorescence of proteins includes CPL of peptides, poly-α-amino acids, tyrosine and tryptophan residues in proteins, complexes of proteins with functional non-fluorescent agents, and protein conformation perturbation. CPL of fluorescent agents in protein complexes addresses to artificial probes, enzymatic cofactors, bilirubin, lanthanides and light-harvesting chlorophyll-protein complex of photosynthetic photosystem II of higher plants.

Keywords

Human Serum Albumin Circular Dichroism Aromatic Amino Acid Ground Electronic State Excited Electronic State 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    H. Wynberg, E. W. Meijer, J. C. Hummelen, H. P. J. M. Dekkers, P. H. Schippers, and A. B. Carlson, Circular polarization observed in bioluminescence. Nature, 286, 641–642 (1980).CrossRefGoogle Scholar
  2. 2.
    H. Wynberg, H. Numan, and H. P. J. M. Dekkers, The detection of optical activity in chemiluminescence. J. Am. Chem. Soc., 99, 3870–3871 (1977).CrossRefGoogle Scholar
  3. 3.
    E. Peeters, M. P. T. Christiaans, R. A. J. Janssen, H. F. M. Schoo, H. P. J. M. Dekkers, and E. W. Meijer, Circularly polarized electroluminescence from a polymer light-emitting diode. J. Am. Chem. Soc., 119, 9909–9910 (1997).CrossRefGoogle Scholar
  4. 4.
    I. Z. Steinberg, Circular polarization of luminescence: Biochemical and biophysical applications. Annu. Rev. Biophys. Bioeng., 7, 113–137 (1978).PubMedCrossRefGoogle Scholar
  5. 5.
    A. Salam, A quantum electromagnetic theory of induced circularly polarized luminescence. Chem. Phys., 173, 123–132 (1993).CrossRefGoogle Scholar
  6. 6.
    J. P. Riehl and F. S. Richardson, General theory of circularly polarized emission and magnetic circularly polarized emission from molecular system. J. Chem. Phys., 65, 1011–1021 (1976).CrossRefGoogle Scholar
  7. 7.
    I. Z. Steinberg, Fluorescence polarization: Some trends and problems. In Biochemical fluorescence: Concepts, Edited by R. Chen and H. Edelhoch, Marcel Dekker, New York (1974) pp. 79–113.Google Scholar
  8. 8.
    I. Z. Steinberg, J. Schlessinger, and A. Gafni, Application of circular polarization of luminescence to the study of peptides, polypeptides, and proteins. In Peptides, polypeptides and proteins, Edited by E. R. Blout, F. A. Bovey, M. Goodman, and N. Lotan, Wiley, New York (1974) pp. 351–369.Google Scholar
  9. 9.
    I. Z. Steinberg, Circularly polarized luminescence. Methods Enzymol., 49, 179–198 (1978).PubMedCrossRefGoogle Scholar
  10. 10.
    J. P. Riehl and F. S. Richardson, Circularly polarized luminescence spectroscopy. Chem. Rev., 86, 1–16 (1986).CrossRefGoogle Scholar
  11. 11.
    J. P. Riehl and F. S. Richardson, Circularly polarized luminescence. Methods Enzymol., 226, 539–553 (1993).PubMedCrossRefGoogle Scholar
  12. 12.
    J. P. Riehl and G. Muller, Circularly polarized luminescence spectroscopy from lanthanide systems. Handb. Phys. Chem. Rare Earths, 34, 289–357 (2005).CrossRefGoogle Scholar
  13. 13.
    F. S. Richardson and J. P. Riehl, Circularly polarized luminescence spectroscopy. Chem. Rev., 77, 773–792 (1977).CrossRefGoogle Scholar
  14. 14.
    H. G. Brittain, Excited-state optical activity. In Molecular luminescence spectroscopy: Methods and applications, vol. 77, Part 1, Edited by S. G. Schulman, Willey, New York (1985) pp. 583–620.Google Scholar
  15. 15.
    J. A. Schauerte, A. Gafni, and D. G. Steel, Improved differentiation between luminescence decay components by use of time-resolved optical activity measurements and selective lifetime modulation. Biophys. J., 70, 1996–2000 (1996).PubMedCrossRefGoogle Scholar
  16. 16.
    J. A. Schaurte, B. D. Schlyer, D. G. Steel, and A. Gafni, Nanosecond time-resolved circular polarization of fluorescence: Study of NADN bound to horse liver alcohol dehydrogenate. Proc. Natl. Acad. Sci. U S A, 92, 569–573 (1995).CrossRefGoogle Scholar
  17. 17.
    H. G. Brittain, Excited-state optical activity, 1987–1995. Chirality, 8, 357–363 (1996).CrossRefGoogle Scholar
  18. 18.
    H. G. Brittain, Excited state optical activity, 1983–1986. Photochem. Photobiol., 46, 1027–1034 (1987).CrossRefGoogle Scholar
  19. 19.
    I. Z. Steinberg and A. Gafni, Sensitive instrument for study of circular polarization of luminescence, Rev. Sci. Instrum., 43, 409–413 (1972).CrossRefGoogle Scholar
  20. 20.
    C. K. Luk and F. S. Richardson, Circularly polarized luminescence and energy transfer studies on carboxylic acid complex of Europium(III) and Terbium(III) in solution. J. Am. Chem. Soc., 97, 6666–6675 (1975).CrossRefGoogle Scholar
  21. 21.
    V. Barzda, M. Ionov, H. van Amerongen, E. E. Gussakovsky, and Y. Shahak, The effect of pea chloroplast alignment and variation of excitation wavelength on circularly polarized chlorophyll luminescence. J. Fluoresc., 14, 207–216 (2004).PubMedCrossRefGoogle Scholar
  22. 22.
    P. H. Schippers, A. van den Beukel, and H. P. J. Dekkers, An accurate digital instrument for the measurement of circular polarization of luminescence. J. Phys. E Sci. Instrum., 15, 945–950 (1982).CrossRefGoogle Scholar
  23. 23.
    J. P. Riehl and N. Coruh, Circularly polarized luminescence from Eu(III) as a probe of metal-ion binding sits in calcium-binding proteins. Eur. J. Solid State Inorg. Chem., 28, 263–266 (1991).Google Scholar
  24. 24.
    J. A. Schaurte, D. G. Steel, and A. Gafni, Time-resolved circularly polarized protein phosphorescence. Proc. Natl. Acad. Sci. U S A, 89, 10154–10158 (1992).CrossRefGoogle Scholar
  25. 25.
    R. B. Rexwinkel, P. Schakel, S. C. J. Meskers, and H. P. J. M. Dekkers, Time-resolved polarization of luminescence spectroscopy: An accurate and versatile digital instrument for the sub-ms time domain. Appl. Spectrosc., 47, 731–740 (1993).CrossRefGoogle Scholar
  26. 26.
    I. Z. Steiberg, Device for calibrating instrument that measures circular dichroism or circularly polarized luminescence, U.S. Patent 4003663 (1975); http://www.freepatentsonline.com/4003663.html.
  27. 27.
    C. J. Bartett, A. F. Drake, and S. F. Mason, The polarized luminescence and vibrational optical activity of calycanthine. Bull. Soc. Chim. Belg., 88, 853–862 (1979).CrossRefGoogle Scholar
  28. 28.
    H. G. Brittain, Circularly polarized luminescence studies of the ternary complexes formed between Terbium(III), pyridine-2,6-dicarboxylic acid, and amino acids. J. Am. Chem. Soc., 102, 3693–3698 (1980).CrossRefGoogle Scholar
  29. 29.
    C. K. Luk and F. S. Richardson, Circularly polarized luminescence spectrum of camphorquinone. J. Am. Chem. Soc., 96, 2006–2009 (1974).CrossRefGoogle Scholar
  30. 30.
    H. G. Brittain and F. S. Richardson, Circularly polarized emission studies on the chiral nuclear magnetic resonance lanthanide shift reagent Tris(3-trifluoroacetyl-d-camphorato)europium(III). J. Am. Chem. Soc., 98, 5858–5863 (1976).CrossRefGoogle Scholar
  31. 31.
    H. P. J. M. Dekkers, P. F. Moraal, J. M. Timper, and J. P. Riehl, Optical artifacts in circularly polarized luminescence spectroscopy. Appl. Spectrosc., 39, 818–821 (1985).CrossRefGoogle Scholar
  32. 32.
    N. Steinberg, A. Gafni, and I. Z. Steinberg, Measurement of the optical activity of triplet-singlet transitions. The circular polarization of phosphorescence of camphorquinone and benzophenone. J. Am. Chem. Soc., 103, 1636–1640 (1981).CrossRefGoogle Scholar
  33. 33.
    E. A. Burstein, Intrinsic luminescence of protein. Nature and application, In Biophysics, vol. 7, Edited by V. D. Milgram, VINITI, Moscow (1977) p. 189.Google Scholar
  34. 34.
    E. A. Permyakov, Luminescent spectroscopy of proteins, CRC Press, Boca Raton (1993).Google Scholar
  35. 35.
    J. Schlessinger, A. Gafni, and I. Z. Steinberg, Optical rotatory power in the ground state and electronically excited state of diketopiperazines containing aromatic side chains. J. Am. Chem. Soc., 96, 7396–7400 (1974).CrossRefGoogle Scholar
  36. 36.
    J. B. A. Ross, W. R. Laws, K. W. Rouslang, and H. R. Wyssbrod, Tyrosine fluorescence and phosphorescence from protein and polypeptides. In Topics in fluorescence spectroscopy, Vol. 3, Biochemical applications, Edited by J. R. Lakowich, Plenum press, New York (1992) pp. 1–63.Google Scholar
  37. 37.
    S. S. Lehrer and G. D. Fasman, Fluorescence studies on poly-α-amino acids. II. Conformation-dependent eximer emission band in poly-L-tyrosine and poly-L-tryptophan. Biopolymers, 2, 199–203 (1964).CrossRefGoogle Scholar
  38. 38.
    J. W. Longworth, Conformations and interactions of excited states. II. Polystyrene, polypeptides, and proteins. Biopolymers, 4, 1131–1148 (1966).PubMedCrossRefGoogle Scholar
  39. 39.
    G. D. Fasman, The road from poly(α-amino acids) to the prediction of protein conformation, Biopolymers, 26, S59–S79 (1987).PubMedCrossRefGoogle Scholar
  40. 40.
    K. Lotte, R. Plessow, and A. Brockhinke, Static and time-resolved fluorescence investigations of tryptophan analogues – a solvent study. Photochem. Photobiol. Sci., 3, 348–359 (2004).PubMedCrossRefGoogle Scholar
  41. 41.
    M. Sisido, S. Egusa, A. Okamoto, and Y. Imanishi, Circularly polarized fluorescence of aromatic (α-amino acids). J. Am. Chem. Soc., 105, 3351–3352 (1983).CrossRefGoogle Scholar
  42. 42.
    M. Sisido, S. Egusa, and Y. Imanishi, One-dimensional aromatic crystal in solution. 1. Synthesis, conformation, and spectroscopic properties of poly(L-1-naphthylalanine). J. Am. Chem. Soc., 105, 1041–1049 (1983).CrossRefGoogle Scholar
  43. 43.
    M. Sisido, S. Egusa, and Y. Imanishi, One-dimensional aromatic crystal in solution. 2. Synthesis, conformation, and spectroscopic properties of poly(L-2-naphthylalanine). J. Am. Chem. Soc., 105, 4077–4082 (1983).CrossRefGoogle Scholar
  44. 44.
    T. Keleti, The excimer fluorescence of tryptophan, tyrosine and D-glyceraldehyde-3-phosphate dehydrogenase. FEBS Lett., 7, 280–282 (1970).PubMedCrossRefGoogle Scholar
  45. 45.
    E. A. Burstein, N. S. Vedenkina, and M. N. Ivkova, Fluorescence and the location of tryptophan residues in protein molecules. Photochem. Photobiol., 18, 263–279 (1973).PubMedCrossRefGoogle Scholar
  46. 46.
    Y. K. Reshetnyak, Y. Koshevnik, and E. A. Burstein, Decomposition of protein tryptophan fluorescence spectra into log-normal components. III. Correlation between fluorescence and microenvironment parameters of individual tryptophan residues. Biophys. J., 81, 1735–1758 (2001).PubMedCrossRefGoogle Scholar
  47. 47.
    Ya. K. Reshetnyak and E. A. Burstein, Decomposition of protein tryptophan fluorescence spectra into log-normal components. II. The statistical proof of discreteness of tryptophan classes in proteins. Biophys. J., 81, 1710–1734 (2001).PubMedCrossRefGoogle Scholar
  48. 48.
    J. Schlessinger, R. S. Roche, and I. Z. Steinberg, A study of subtilisin types Novo and Carlsberg by circular polarization of fluorescence. Biochemistry, 14, 255–262 (1975).PubMedCrossRefGoogle Scholar
  49. 49.
    E. E. Gussakovsky and E. Haas, Two steps in the transition between the native and acid states of bovine α-lactalbumin detected by circular polarization of luminescence: Evidence for a premolten globule state? Protein Sci., 4, 2319–2326 (1995).PubMedCrossRefGoogle Scholar
  50. 50.
    P. B. Sommers and M. J. Kronman, Comparative fluorescence properties of bovine, goat, human and guinea pig α-lactalbumins. Characterization of the environment of individual tryptophan residues in partially folded conformers. Biophys. Chem., 11, 217–232 (1980).PubMedCrossRefGoogle Scholar
  51. 51.
    J. Schlessinger and A. Levitzki, Molecular basis of negative co-operativity in rabbit muscle glyceraldehyde-3-phosphate dehydrogenase. J. Mol. Biol., 82, 547–561 (1974).PubMedCrossRefGoogle Scholar
  52. 52.
    J. Schlessinger, I. Z. Steinberg, D. Givol, and J. Hockman, Subunit interaction in antibodies and antibody fragments studies by circular polarization of fluorescence. FEBS Lett., 52, 231–235 (1975).PubMedCrossRefGoogle Scholar
  53. 53.
    J. Schlessinger, I. Z. Steinberg, D. Givol, J. Hockman, and I. Pecht, Antigen-induced conformational changes in antibodies and their Fab’ fragments studied by circular polarization of fluorescence. Proc. Natl. Acad. Sci. U S A, 72, 2775–2779 (1975).PubMedCrossRefGoogle Scholar
  54. 54.
    J. -C. Jaton, H. H. Diemar, G. Braun, D. Givol, I. Pecht, and J. Schlessinger, Conformational changes induced in a homogeneous anti-type III Pneumococcal antibody by oligosaccharides of increasing size. Biochemistry, 14, 5312–5315 (1975).PubMedCrossRefGoogle Scholar
  55. 55.
    J. Schlessinger and I. Z. Steinberg, Circular polarization of fluorescence of probes bound to chymotrypsin. Change in asymmetric environment upon electronic excitation. Proc. Natl. Acad. Sci. U S A, 69, 769–772 (1972).PubMedCrossRefGoogle Scholar
  56. 56.
    W. O. McClure and G. M. Edelman, Fluorescent probes for conformational states of proteins. I. Mechanism of fluorescence of 2-p-toluidinylnaphthalene-6-sulfonate, a hydrophobic probe. Biochemistry, 5, 1908–1919 (1966).PubMedCrossRefGoogle Scholar
  57. 57.
    G. E. Dobretsov, Fluorescent probes in investigation of cells, membranes and lipoproteins, Nauka, Moscow (1989).Google Scholar
  58. 58.
    K. Kuwajima, M. Mityani, and S. Sugai, Characterization of the critical state in protein folding. Effects of guanidine hydrochloride and specific Ca2+ binding on the folding kinetics of α-lactalbumin. J. Mol. Biol., 206, 547–561 (1989).PubMedCrossRefGoogle Scholar
  59. 59.
    J. Schlessinger, I. Z. Steinberg, and I. Pecht, Antibody–hapten interactions: Circular and linear polarization of the fluorescence of dansyl bound to anti-dansyl antibodies. J. Mol. Biol., 87, 725–740 (1974).PubMedCrossRefGoogle Scholar
  60. 60.
    J. Schlessinger, I. Z. Steinberg, and A. Levitzki, A comparative study of NAD+ binding sites of dehydrogenases by circular polarization of fluorescence. J. Mol. Biol., 91, 523–528 (1975).PubMedCrossRefGoogle Scholar
  61. 61.
    A. Gafni, Location of age-related modifications in rat muscle glyceraldehydes-3-phosphate dehydrogenase. J. Biol. Chem., 256, 8875–8877 (1981).PubMedGoogle Scholar
  62. 62.
    A. Gafni, Circular dichroism and circular polarization of luminescence of reduced nicotinamide adenine dinucleotide in solution and bound to dehydrogenases. Biochemistry, 17, 1301–1304 (1978).PubMedCrossRefGoogle Scholar
  63. 63.
    S. Veinberg, I. Z. Steinberg, and S. Shaltiel, Excited-state vs. ground-state structure of the pyridoxal 5´-phosphate site in glycogen phosphorylase b. In Metabolic interconversion of enzymes, Edited by S. Shaltiel, Springer Verlag, Berlin (1976) pp. 44–49.Google Scholar
  64. 64.
    S. Veinberg, S. Shaltiel, and I. Z. Steinberg, Factors contributing to the absorption and fluorescence characteristics of pyridoxal phosphate in glycogen phosphorylase b. Isr. J. Chem., 12, 421–434 (1974).Google Scholar
  65. 65.
    G. H. Beaven, A. d’Albis, and W. B. Gratzer, The interaction of bilirubin with human serum albumin. Eur. J. Biochem., 33, 500–510 (1973).CrossRefGoogle Scholar
  66. 66.
    C. D. Tran and G. S. Beddard, Interactions between bilirubin and albumin using picosecond fluorescence and circularly polarized luminescence spectroscopy. J. Am. Chem. Soc., 104, 6741–6747 (1982).CrossRefGoogle Scholar
  67. 67.
    R. F. Chen, Fluorescence stopped-flow study of relaxation process in the binding of bilirubin to serum albumin. Arch. Biochem. Biophys., 160, 106–112 (1974).PubMedCrossRefGoogle Scholar
  68. 68.
    C. D. Tran and A. F. Drake, Circularly polarized luminescence of bilirubin bound to human serum albumin. Biochem. Biophys. Res. Commun., 101, 76–82 (1981).PubMedCrossRefGoogle Scholar
  69. 69.
    C. D. Tran and G. S. Beddard, Excited state properties of bilirubin and its photoproducts using picosecond fluorescence and circularly polarized luminescence spectroscopy. Biochim. Biophys. Acta, 678, 497–504 (1981).Google Scholar
  70. 70.
    G. Blauer and G. Wagniere, Conformation of bilirubin and biliverdin in their complex with serum albumin. J. Am. Chem. Soc., 97, 1949–1954 (1975).PubMedCrossRefGoogle Scholar
  71. 71.
    E. Yoshimura and T. Watanabe, Lanthanide ions as probes in studies of metal ion-dependent enzymes. In Metal ions in biological systems, Vol. 40, Edited by A. Sigel and H. Sigel, Marcel Dekker, New York (2003) pp. 161–189.Google Scholar
  72. 72.
    C. F. G. C. Geraldes and C. Luchinat, Lanthanides as shift and relaxation agents in elucidating the structure of proteins and nucleic acids. In Metal ions in biological systems, Vol. 40, Edited by A. Sigel and H. Sigel, Marcel Dekker, New York (2003) pp. 513–588.Google Scholar
  73. 73.
    R. B. Martin and F. S. Richardson, Lanthanides as probes for calcium in biological systems. Q. Rev. Biophys., 12, 181–209 (1979).PubMedCrossRefGoogle Scholar
  74. 74.
    R. B. Martin, Bioinorganic chemistry of calcium. In Metal ions in biological systems, Vol. 17, Edited by H. Sigel, Marcel Dekker, New York (1984) pp. 1–49.Google Scholar
  75. 75.
    T. Moeller, The chemistry of the lanthanides, Reinhold, New York (1963).Google Scholar
  76. 76.
    A. E. Martell and R. M. Smith, Critical stability constants, Plenum, New York (1989).Google Scholar
  77. 77.
    S. -J. Lin, E. Yoshimura, H. Sakai, T. Wakagi and H. Matsuzawa, Weakly bound calcium ions involved in the thermostability of aqualysin I, a heat-stable subtilisin-type protease from Thermus aquaticus YT-1. Biochim. Biophys. Acta, 1433, 132–138 (1999).PubMedGoogle Scholar
  78. 78.
    F. S. Richardson, Terbium(III) and Europium(III) ions as luminescent probes and stains for biomolecular systems. Chem. Rev., 82, 541–552 (1982).CrossRefGoogle Scholar
  79. 79.
    D. W. Darnall, F. Abbott, J. E. Gomez, and E. R. Birnbaum, Fluorescence energy-transfer measurements between the calcium binding site and specificity pocket of bovine trypsin using lanthanide probes. Biochemistry, 15, 56017–5023 (1976).CrossRefGoogle Scholar
  80. 80.
    H. G. Brittain, F. S. Richardson, and R. B. Martin, Terbium(III) emission as a probe of calcium(II) binding sites in proteins. J. Am. Chem. Soc., 98, 8255–8260 (1976).PubMedCrossRefGoogle Scholar
  81. 81.
    C. K. Luk and F. S. Richardson, Circularly polarized luminescence of Terbium(III) complexes in solution. Chem. Phys. Lett., 25, 215–220 (1974).CrossRefGoogle Scholar
  82. 82.
    H. G. Brittain and F. S. Richardson, pH dependence of circularly polarized emission and total emission from Europium(III)/L-malic acid and Europium(III)/L-malic acid/Terbium(III) complexes in H2O and D2O solutions. Inorg. Chem., 15, 1507–1511 (1976).CrossRefGoogle Scholar
  83. 83.
    D. H. Metcalf, S. W. Snyder, J. N. Demas, and F. S. Richardson, Excited-state racemization kinetics and chiroptical activity of labile metal complex in aqueous solution. Time-resolved circularly polarized luminescence study of Eu(dpa)3 3– in H2O and D2O. J. Am. Chem. Soc., 17, 469–479 (1990).CrossRefGoogle Scholar
  84. 84.
    S. C. J. Meskers, M. Ubbink, G. W. Canters, H. P. J. M. Dekkers, pH dependence of the enantioselective excited-state quenching of Λ,Δ-Tb(III) and Λ,Δ-Eu(III)tris(pyridine-2,6-dicarboxylate) chelates by ferricytochrome c form horse heart and ferricytochrome c-550 from Paracoccus versutus. J. Biol. Inorg. Chem., 3, 463–469 (1998).CrossRefGoogle Scholar
  85. 85.
    S. C. J. Meskers, C. Dennison, G. W. Canters, and H. P. J. M. Dekkers, Type I blue copper proteins as enantioselective quenchers of the photoluminescence of Δ,Λ-Eu(pyridine-2,6-dicarboxylate)3 3–: Azurin from Pseudomonas aeruginosa and its Met44→Lys mutant, amicyanin from Paracoccus versutus and parsley plastocyanin. J. Biol. Inorg. Chem., 3, 663–670 (1998).CrossRefGoogle Scholar
  86. 86.
    R. van Grondelle, J. P. Dekker, T. Gillbro, and V. Sundström, Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta, 1187, 1–65 (1994).CrossRefGoogle Scholar
  87. 87.
    W. Kuhlbrandt, D. N. Wang, and Yo. Fujiyoshi, Atomic model of plant light-harvesting complex by electron crystallography. Nature, 367, 614–621 (1994).PubMedCrossRefGoogle Scholar
  88. 88.
    H. van Amerongen, L. Valkunas, and R. van Grondelle, Photosynthetic excitons, World Scientific, Singapore (2000).CrossRefGoogle Scholar
  89. 89.
    G. Garab, Chirally organized macrodomains in thylakoid membranes. Possible structural and regulatory roles. In Light as energy source and information carrier in plant biology, Edited by R. Jennings, NATO ASI/Plenum Publishing, New York (1996) pp. 125–136.Google Scholar
  90. 90.
    G. Garab, S. Wells, L. Finzi, and C. Bustamante, Helically organized macroaggregates of pigment-protein complexes in chloroplasts: Evidence from circular intensity differential scattering. Biochemistry, 27, 5839–5843 (1988).PubMedCrossRefGoogle Scholar
  91. 91.
    A. Gafni, H. Hardt, J. Schlessinger, and I. Z. Steinberg, Circular polarization of fluorescence of chlorophyll in solution and native structures. Biochim. Biophys. Acta, 387, 256–264 (1975).PubMedCrossRefGoogle Scholar
  92. 92.
    E. E. Gussakovsky, V. Barzda, H. van Amerongen, R. van Grondell, and Y. Shahak, Circular polarization of luminescence and circular dichroism at varied structural organization of grana in pea chloroplasts. In Photosynthesis: Mechanisms and effects. Vol. 1, Edited by G. Garab, Kluwer Academic Publisher, Dordrecht (1998) pp. 317–320.Google Scholar
  93. 93.
    E. E. Gussakovsky, Y. Shahak, H. van Amerongen, and V. Barzda, Circularly polarized chlorophyll luminescence reflect the macro-organization of grana in pea chloroplasts. Photosynth. Res., 65, 83–92 (2000).PubMedCrossRefGoogle Scholar
  94. 94.
    E. E. Gussakovsky, B. A. Salakhutdinov, and Y. Shahak, Chiral macroaggregates of LHCII detected by circularly polarized luminescence in intact pea leaves are sensitive to drought stress. Funct. Plant Biol., 29, 955–963 (2002).CrossRefGoogle Scholar
  95. 95.
    E. E. Gussakovsky, B. Salakhutdinov, and Y. Shahak, Monitoring chiral macroaggregates of LHCII: From isolated chloroplasts to green leaves. PS2001 Proceedings: 12 th International Congress on Photosynthesis, CSIRO, Brisbane, Australia, S31-007, p. 5 (2002).Google Scholar
  96. 96.
    E. E. Gussakovsky, Y. Shahak, and D. F. Schroeder, Color of illumination during growth affects LHCII chiral macroaggregates in pea plant leaves. J. Photochem. Photobiol. B, 86, 121–130 (2007).PubMedCrossRefGoogle Scholar
  97. 97.
    E. E. Gussakovsky and Y. Shahak, LHCII chiral macroaggregates in intact leaves and isolated chloroplasts. The CPL studies. In Photosynthesis: Fundumental aspects to global perspectives, Edited by A. van der Est and D. Bruce, Montreal Allen Press Inc., Lawrence, Kansas, USA (2005) pp. 153–154.Google Scholar
  98. 98.
    E. E. Gussakovsky, M. V. Ionov, Yu. E. Giller, K. Ratner, T. F. Aripov, and Y. Shahak, Left- and right-handed LHCII macroaggregates revealed by circularly polarized chlorophyll luminescence. Photosynth. Res., 87, 253–265 (2006).PubMedCrossRefGoogle Scholar
  99. 99.
    A. Grinvald, J. Schlessinger, I. Pecht, and I. Z. Steinberg, Homogeneity and variability in the structure of azurin molecules studied by fluorescence decay and circular polarization. Biochemistry, 14, 1921–1929 (1975).PubMedCrossRefGoogle Scholar
  100. 100.
    H. Donato, Jr., and R. B. Martin, Conformations of carp muscle calcium binding parvalbumin. Biochemistry, 13, 4575–4579 (1974).PubMedCrossRefGoogle Scholar
  101. 101.
    A. Gafni and I. Z. Steinberg, Optical activity of terbium ions bound to transferring and conalbumin studied by circular polarization of luminescence. Biochemistry, 13, 800–803 (1974).PubMedCrossRefGoogle Scholar
  102. 102.
    N. Coruh, G. L. Hilmes, and J. P. Riehl, Application of circularly polarized luminescence spectroscopy to biochemical systems. J. Luminesc., 40&41, 227–228 (1988).CrossRefGoogle Scholar
  103. 103.
    N. Coruh and J. P. Riehl, Circularly polarized luminescence from Terbium(III) as a probe of metal ion binding in calcium-binding proteins. Biochemistry, 31, 7970–7976 (1992).PubMedCrossRefGoogle Scholar
  104. 104.
    N. Coruh and J. P. Riehl, Circularly polarized luminescence as a probe of metal ions binding sites in calmodulin. Collect. Czech. Chem. Commun., 56, 3028–3031 (1991).CrossRefGoogle Scholar
  105. 105.
    S. Abdollahi, W. R. Harris, and J. P. Riehl, Application of circularly polarized luminescence spectroscopy to Tb(III) and Eu(III) complexes of transferrins. J. Phys. Chem., 100, 1950–1956 (1996).CrossRefGoogle Scholar
  106. 106.
    T. L. Miller, D. J. Nelson, H. G. Brittain, F. S. Richardson, and R. B. Martin, Calcium binding site of rabbit troponin and carp parvalbumin. FEBS Lett., 58, 262–264 (1975).PubMedCrossRefGoogle Scholar
  107. 107.
    M. Epstein, J. Reuben, and A. Levitzki, Calcium binding site of trypsin as probed by lanthanides. Biochemistry, 16, 2449–2457 (1977).PubMedCrossRefGoogle Scholar
  108. 108.
    S. C. J. Meskers, M. Ubbink, G. W. Canters, and H. P. J. M. Dekkers, Chiral recognition between dissymmetric Tb- and Eu(pyridine-2,6-dicarboxylate)3 3– complex and Fe(III) proteins in aqueous solution. Luminescence quenching by cytochrome c from horse heart and cytochrome c-550 from Thiobacillus versutus and its Lys14→Glu- and Lys99→Glu mutants. J. Phys. Chem., 100, 17957–17969 (1996).CrossRefGoogle Scholar
  109. 109.
    H. G. Brittain, F. S. Richardson, R. B. Martin, L. D. Burtnick, and C. M. Kay, Circularly polarized emission of terbium(III) substituted bovine cardiac troponin-C. Biochem. Biophys. Res. Commun., 68, 1013–1019 (1976).PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Eugene Gussakovsky
    • 1
  1. 1.National Research Council Canada, Institute for BiodiagnosticsWinnipegCanada

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