Biochemistry (Moscow)

, 76:497 | Cite as

Fluorescence correlation spectroscopy in biology, chemistry, and medicine

  • I. V. Perevoshchikova
  • E. A. Kotova
  • Y. N. Antonenko
Review

Abstract

This review describes the method of fluorescence correlation spectroscopy (FCS) and its applications. FCS is used for investigating processes associated with changes in the mobility of molecules and complexes and allows researchers to study aggregation of particles, binding of fluorescent molecules with supramolecular complexes, lipid vesicles, etc. The size of objects under study varies from a few angstroms for dye molecules to hundreds of nanometers for nanoparticles. The described applications of FCS comprise various fields from simple chemical systems of solution/micelle to sophisticated regulations on the level of living cells. Both the methodical bases and the theoretical principles of FCS are simple and available. The present review is concentrated preferentially on FCS applications for studies on artificial and natural membranes. At present, in contrast to the related approach of dynamic light scattering, FCS is poorly known in Russia, although it is widely employed in laboratories of other countries. The goal of this review is to promote the development of FCS in Russia so that this technique could occupy the position it deserves in modern Russian science.

Key words

fluorescence fluctuations correlation spectroscopy diffusion aggregation binding nanoparticles biopolymers vesicles ligands receptors conformational changes nucleic acid and protein folding 

Abbreviations

DNP

2,4-dinitrophenol

FCS

fluorescence correlation spectroscopy

G(τ)

autocorrelation function

PCH

photon counting histogram

TMRE

tetramethylrhodamine ethyl ester

τd

diffusion time

References

  1. 1.
    Kask, P., and Kyandler, T. (1978) Izv. AN ESSR, 27, 73–78.Google Scholar
  2. 2.
    Kask, P., Kyandler, T., Sirk, A., Karu, T., and Lippmaa, E. (1979) Izv. AN ESSR, 28, 221–226.Google Scholar
  3. 3.
    Kyandler, T., Kask, P., Piksarv, P., Sirk, A., and Lippmaa, E. (1982) Izv. AN ESSR, 31, 314–319.Google Scholar
  4. 4.
    Kyandler, T. E. (1985) Fluorescence Correlation Spectroscopy in Studies on Dynamics of Chemical Systems: Candidate’s dissertation [in Russian], Tartu State University, Tartu.Google Scholar
  5. 5.
    Kask, P., Piksarv, P., Mets, U., Pooga, M., and Lippmaa, E. (1987) Eur. Biophys. J., 14, 257–261.PubMedCrossRefGoogle Scholar
  6. 6.
    Kask, P., Piksarv, P., Pooga, M., Mets, U., and Lippmaa, E. (1989) Biophys. J., 55, 213–220.PubMedCrossRefGoogle Scholar
  7. 7.
    Kask, P. (1987) Stud. Biophys., 118, 7–24.Google Scholar
  8. 8.
    Rigler, R., and Elson, E. (eds.) (2001) Fluorescence Correlation Spectroscopy: Theory and Applications, Springer, N. Y.Google Scholar
  9. 9.
    Eigen, M., and Rigler, R. (1994) Proc. Natl. Acad. Sci. USA, 91, 5740–5747.PubMedCrossRefGoogle Scholar
  10. 10.
    Schwille, P. (2001) Cell. Biochem. Biophys., 34, 383–408.PubMedCrossRefGoogle Scholar
  11. 11.
    Krichevsky, O., and Bonnet, G. (2002) Rep. Prog. Phys., 65, 251–297.CrossRefGoogle Scholar
  12. 12.
    Hess, S. T., Huang, S., Heikal, A. A., and Webb, W. W. (2002) Biochemistry, 41, 697–705.PubMedCrossRefGoogle Scholar
  13. 13.
    Sengupta, P., Balaji, J., and Maiti, S. (2002) Methods, 27, 374–387.PubMedCrossRefGoogle Scholar
  14. 14.
    Enderlein, J., Gregor, I., Patra, D., and Fitter, J. (2004) Curr. Pharm. Biotechnol., 5, 155–161.PubMedCrossRefGoogle Scholar
  15. 15.
    Gosch, M., and Rigler, R. (2005) Adv. Drug Deliv. Rev., 57, 169–190.PubMedCrossRefGoogle Scholar
  16. 16.
    Briddon, S. J., and Hill, S. J. (2007) Trends Pharmacol. Sci., 28, 637–645.PubMedCrossRefGoogle Scholar
  17. 17.
    Kim, S. A., Heinze, K. G., and Schwille, P. (2007) Nat. Methods, 4, 963–973.PubMedCrossRefGoogle Scholar
  18. 18.
    Machan, R., and Hof, M. (2010) Biochim. Biophys. Acta, 1798, 1377–1391.PubMedCrossRefGoogle Scholar
  19. 19.
    Petrasek, Z., Ries, J., and Schwille, P. (2010) Meth. Enzymol., 472, 317–343.PubMedCrossRefGoogle Scholar
  20. 20.
    Garcia-Saez, A. J., and Schwille, P. (2010) Biochim. Biophys. Acta, 1798, 766–776.PubMedCrossRefGoogle Scholar
  21. 21.
    Serdyuk, I. N., Zaccai, N. R., and Zaccai, J. (2007) in Methods in Molecular Biophysics: Structure, Dynamics, Function, Cambridge University Press, Cambridge.Google Scholar
  22. 22.
    Sukharev, V. I., and Vekshin, N. L. (2000) Bioorg. Khim., 26, 723–727.PubMedGoogle Scholar
  23. 23.
    Kovalev, A. E., Yakovenko, A. A., and Vekshin, N. L. (2004) Biofizika, 49, 1030–1037.PubMedGoogle Scholar
  24. 24.
    Tatarkova, S. A., Lloid, K., Hara, S. K., and Berk, D. (2003) Kvant. Elektron., 33, 357–362.CrossRefGoogle Scholar
  25. 25.
    Vekshin, N. L. (2006) Fluorescence Spectroscopy of Biopolymers [in Russian], Foton-Vek, Pushchino.Google Scholar
  26. 26.
    Perevoshchikova, I. V., Sorochkina, A. I., Zorov, D. B., and Antonenko, Yu. N. (2009) Biochemistry (Moscow), 74, 663–671.CrossRefGoogle Scholar
  27. 27.
    Strakhovskaya, M. G., Antonenko, Yu. N., Pashkovskaya, A. A., Kotova, E. A., Kireev, V., Zhukhovitsky, V. G., Kuznetsova, N. A., Yuzhakova, O. A., Negrimovsky, V. M., and Rubin, A. B. (2009) Biochemistry (Moscow), 74, 1305–1314.CrossRefGoogle Scholar
  28. 28.
    Magde, D., Elson, E. L., and Webb, W. W. (1972) Phys. Rev. Lett., 29, 705–708.CrossRefGoogle Scholar
  29. 29.
    Elson, E. L., and Magde, D. (1974) Biopolymers, 13, 1–27.CrossRefGoogle Scholar
  30. 30.
    Magde, D., Elson, E. L., and Webb, W. W. (1974) Biopolymers, 13, 29–61.PubMedCrossRefGoogle Scholar
  31. 31.
    Magde, D., Webb, W. W., and Elson, E. L. (1978) Biopolymers, 17, 361–376.CrossRefGoogle Scholar
  32. 32.
    Ehrenberg, M., and Rigler, R. (1974) Chem. Phys., 4, 390–401.CrossRefGoogle Scholar
  33. 33.
    Ehrenberg, M., and Rigler, R. (1976) Q. Rev. Biophys., 9, 69–81.PubMedCrossRefGoogle Scholar
  34. 34.
    Aragon, S. R., and Pecora, R. (1975) Biopolymers, 14, 119–138.CrossRefGoogle Scholar
  35. 35.
    Koppel, D. E., Axelrod, D., Schlessinger, J., Elson, E. L., and Webb, W. W. (1976) Biophys. J., 16, 1315–1329.PubMedCrossRefGoogle Scholar
  36. 36.
    Aragon, S. R., and Pecora, R. (1976) J. Chem. Phys., 64, 1791–1803.CrossRefGoogle Scholar
  37. 37.
    Webb, W. W. (1976) Q. Rev. Biophys., 9, 49–68.PubMedCrossRefGoogle Scholar
  38. 38.
    Fahey, P. F., Koppel, D. E., Barak, L. S., Wolf, D. E., Elson, E. L., and Webb, W. W. (1977) Science, 195, 305–306.PubMedCrossRefGoogle Scholar
  39. 39.
    Rigler, R., Mets, U., Widengren, J., and Kask, P. (1993) Eur. Biophys. J., 22, 169–175.CrossRefGoogle Scholar
  40. 40.
    Rigler, R., Pramanik, A., Jonasson, P., Kratz, G., Jansson, O. T., Nygren, P., Stahl, S., Ekberg, K., Johansson, B., Uhlen, S., Uhlen, M., Jornvall, H., and Wahren, J. (1999) Proc. Natl. Acad. Sci. USA, 96, 13318–13323.PubMedCrossRefGoogle Scholar
  41. 41.
    Denk, W., Strickler, J. H., and Webb, W. W. (1990) Science, 248, 73–76.PubMedCrossRefGoogle Scholar
  42. 42.
    Schwille, P., Haupts, U., Maiti, S., and Webb, W. W. (1999) Biophys. J., 77, 2251–2265.PubMedCrossRefGoogle Scholar
  43. 43.
    Koppel, D. E. (1974) Phys. Rev. A, 10, 1938–1945.CrossRefGoogle Scholar
  44. 44.
    Kask, P., Gunther, R., and Axhausen, P. (1997) Eur. Biophys. J., 25, 163–169.CrossRefGoogle Scholar
  45. 45.
    Qian, H. (1990) Biophys. Chem., 38, 49–57.PubMedCrossRefGoogle Scholar
  46. 46.
    Meseth, U., Wohland, T., Rigler, R., and Vogel, H. (1999) Biophys. J., 76, 1619–1631.PubMedCrossRefGoogle Scholar
  47. 47.
    Kask, P., Palo, K., Ullmann, D., and Gall, K. (1999) Proc. Natl. Acad. Sci. USA, 96, 13756–13761.PubMedCrossRefGoogle Scholar
  48. 48.
    Chen, Y., Muller, J. D., So, P. T., and Gratton, E. (1999) Biophys. J., 77, 553–567.PubMedCrossRefGoogle Scholar
  49. 49.
    Chen, Y., Muller, J. D., Tetin, S. Y., Tyner, J. D., and Gratton, E. (2000) Biophys. J., 79, 1074–1084.PubMedCrossRefGoogle Scholar
  50. 50.
    Enderlein, J., Gregor, I., Patra, D., Dertinger, T., and Kaupp, U. B. (2005) Chemphyschem., 6, 2324–2336.PubMedCrossRefGoogle Scholar
  51. 51.
    Ruettinger, S., Buschmann, V., Kramer, B., Erdmann, R., Macdonald, R., and Koberling, F. (2007) Proc. SPIE, 6630, 66300D.CrossRefGoogle Scholar
  52. 52.
    Sachl, R., Mikhalyov, I., Hof, M., and Johansson, L. B. (2009) Phys. Chem. Chem. Phys., 11, 4335–4343.PubMedCrossRefGoogle Scholar
  53. 53.
    Petrasek, Z., and Schwille, P. (2008) Biophys. J., 94, 1437–1448.PubMedCrossRefGoogle Scholar
  54. 54.
    Gendron, P. O., Avaltroni, F., and Wilkinson, K. J. (2008) J. Fluoresc., 18, 1093–1101.PubMedCrossRefGoogle Scholar
  55. 55.
    Gosch, M., Blom, H., Holm, J., Heino, T., and Rigler, R. (2000) Anal. Chem., 72, 3260–3265.PubMedCrossRefGoogle Scholar
  56. 56.
    Muller, J. D., Chen, Y., and Gratton, E. (2000) Biophys. J., 78, 474–486.PubMedCrossRefGoogle Scholar
  57. 57.
    Qian, H., and Elson, E. L. (1990) Biophys. J., 57, 375–380.PubMedCrossRefGoogle Scholar
  58. 58.
    Eid, J. S., Mueller, J. D., and Gratton, E. (2000) Rev. Sci. Instrum., 71, 361–368.CrossRefGoogle Scholar
  59. 59.
    Chen, Y., Muller, J. D., Ruan, Q., and Gratton, E. (2002) Biophys. J., 82, 133–144.PubMedCrossRefGoogle Scholar
  60. 60.
    Chen, Y., Wei, L. N., and Muller, J. D. (2003) Proc. Natl. Acad. Sci. USA, 100, 15492–15497.PubMedCrossRefGoogle Scholar
  61. 61.
    Egea, P. F., Rochel, N., Birck, C., Vachette, P., Timmins, P. A., and Moras, D. (2001) J. Mol. Biol., 307, 557–576.PubMedCrossRefGoogle Scholar
  62. 62.
    Yu, L., Tan, M., Ho, B., Ding, J. L., and Wohland, T. (2006) Anal. Chim. Acta, 556, 216–225.PubMedCrossRefGoogle Scholar
  63. 63.
    Tjernberg, L. O., Pramanik, A., Bjorling, S., Thyberg, P., Thyberg, J., Nordstedt, C., Berndt, K. D., Terenius, L., and Rigler, R. (1999) Chem. Biol., 6, 53–62.PubMedCrossRefGoogle Scholar
  64. 64.
    Sengupta, P., Garai, K., Sahoo, B., Shi, Y., Callaway, D. J., and Maiti, S. (2003) Biochemistry, 42, 10506–10513.PubMedCrossRefGoogle Scholar
  65. 65.
    Garai, K., Sureka, R., and Maiti, S. (2007) Biophys. J., 92, L55–L57.PubMedCrossRefGoogle Scholar
  66. 66.
    Gerard, M., Debyser, Z., Desender, L., Kahle, P. J., Baert, J., Baekelandt, V., and Engelborghs, Y. (2006) FASEB J., 20, 524–526.PubMedGoogle Scholar
  67. 67.
    Conway, K. A., Harper, J. D., and Lansbury, P. T. (1998) Nat. Med., 4, 1318–1320.PubMedCrossRefGoogle Scholar
  68. 68.
    Sevenich, F. W., Langowski, J., Weiss, V., and Rippe, K. (1998) Nucleic Acids Res., 26, 1373–1381.PubMedCrossRefGoogle Scholar
  69. 69.
    Lagerkvist, A. C., Foldes-Papp, Z., Persson, M. A., and Rigler, R. (2001) Protein Sci., 10, 1522–1528.PubMedCrossRefGoogle Scholar
  70. 70.
    Tetin, S. Y., Swift, K. M., and Matayoshi, E. D. (2002) Anal. Biochem., 307, 84–91.PubMedCrossRefGoogle Scholar
  71. 71.
    Varriale, A., Staiano, M., Iozzino, L., Severino, L., Anastasio, A., Cortesi, M. L., and D’Auria, S. (2009) Protein Pept. Lett., 16, 1425–1428.PubMedCrossRefGoogle Scholar
  72. 72.
    Kinjo, M., and Rigler, R. (1995) Nucleic Acids Res., 23, 1795–1799.PubMedCrossRefGoogle Scholar
  73. 73.
    Schwille, P., Oehlenschlager, F., and Walter, N. G. (1996) Biochemistry, 35, 10182–10193.PubMedCrossRefGoogle Scholar
  74. 74.
    Rusu, L., Gambhir, A., McLaughlin, S., and Radler, J. (2004) Biophys. J., 87, 1044–1053.PubMedCrossRefGoogle Scholar
  75. 75.
    Yu, L., Ding, J. L., Ho, B., and Wohland, T. (2005) Biochim. Biophys. Acta, 1716, 29–39.PubMedCrossRefGoogle Scholar
  76. 76.
    Posokhov, Y. O., Rodnin, M. V., Lu, L., and Ladokhin, A. S. (2008) Biochemistry, 47, 5078–5087.PubMedCrossRefGoogle Scholar
  77. 77.
    Antonenko, Y. N., Perevoshchikova, I. V., Davydova, L. I., Agapov, I. A., and Bogush, V. G. (2010) Biochim. Biophys. Acta, 1798, 1172–1178.PubMedCrossRefGoogle Scholar
  78. 78.
    Clamme, J. P., Azoulay, J., and Mely, Y. (2003) Biophys. J., 84, 1960–1968.PubMedCrossRefGoogle Scholar
  79. 79.
    Pramanik, A., Thyberg, P., and Rigler, R. (2000) Chem. Phys. Lipids, 104, 35–47.PubMedCrossRefGoogle Scholar
  80. 80.
    Takakuwa, Y., Pack, C. G., An, X. L., Manno, S., Ito, E., and Kinjo, M. (1999) Biophys. Chem., 82, 149–155.PubMedCrossRefGoogle Scholar
  81. 81.
    Rhoades, E., Ramlall, T. F., Webb, W. W., and Eliezer, D. (2006) Biophys. J., 90, 4692–4700.PubMedCrossRefGoogle Scholar
  82. 82.
    Krasnovsky, A. A. (2004) Biofizika, 49, 305–321.Google Scholar
  83. 83.
    Valenzeno, D. P. (1987) Photochem. Photobiol., 46, 147–160.PubMedCrossRefGoogle Scholar
  84. 84.
    Pashkovskaya, A. A., Maizlish, V. E., Shaposhnikov, G. P., Kotova, E. A., and Antonenko, Y. N. (2008) Biochim. Biophys. Acta, 1778, 541–548.PubMedCrossRefGoogle Scholar
  85. 85.
    Pashkovskaya, A. A., Perevoshchikova, I. V., Maizlish, V. E., Shaposhnikov, G. P., Kotova, E. A., and Antonenko, Yu. N. (2009) Biochemistry (Moscow), 74, 1021–1026.CrossRefGoogle Scholar
  86. 86.
    Allen, N. W., and Thompson, N. L. (2006) Cytometry A, 69, 524–532.PubMedGoogle Scholar
  87. 87.
    Van den Bogaart, G., Hermans, N., Krasnikov, V., de Vries, A. H., and Poolman, B. (2007) Biophys. J., 92, 1598–1605.PubMedCrossRefGoogle Scholar
  88. 88.
    Ramadurai, S., Holt, A., Krasnikov, V., van den Bogaart, G., Killian, J. A., and Poolman, B. (2009) J. Am. Chem. Soc., 131, 12650–12656.PubMedCrossRefGoogle Scholar
  89. 89.
    Schwille, P., Korlach, J., and Webb, W. W. (1999) Cytometry, 36, 176–182.PubMedCrossRefGoogle Scholar
  90. 90.
    Korlach, J., Schwille, P., Webb, W. W., and Feigenson, G. W. (1999) Proc. Natl. Acad. Sci. USA, 96, 8461–8466.PubMedCrossRefGoogle Scholar
  91. 91.
    Wawrezinieck, L., Rigneault, H., Marguet, D., and Lenne, P. F. (2005) Biophys. J., 89, 4029–4042.PubMedCrossRefGoogle Scholar
  92. 92.
    Humpolickova, J., Gielen, E., Benda, A., Fagulova, V., Vercammen, J., Vandeven, M., Hof, M., Ameloot, M., and Engelborghs, Y. (2006) Biophys. J., 91, L23–L25.PubMedCrossRefGoogle Scholar
  93. 93.
    Wenger, J., Conchonaud, F., Dintinger, J., Wawrezinieck, L., Ebbesen, T. W., Rigneault, H., Marguet, D., and Lenne, P. F. (2007) Biophys. J., 92, 913–919.PubMedCrossRefGoogle Scholar
  94. 94.
    Chiantia, S., Ries, J., and Schwille, P. (2009) Biochim. Biophys. Acta, 1788, 225–233.PubMedCrossRefGoogle Scholar
  95. 95.
    Przybylo, M., Sykora, J., Humpolickova, J., Benda, A., Zan, A., and Hof, M. (2006) Langmuir, 22, 9096–9099.PubMedCrossRefGoogle Scholar
  96. 96.
    Machan, R., and Hof, M. (2010) Int. J. Mol. Sci., 11, 427–457.PubMedCrossRefGoogle Scholar
  97. 97.
    Politz, J. C., Browne, E. S., Wolf, D. E., and Pederson, T. (1998) Proc. Natl. Acad. Sci. USA, 95, 6043–6048.PubMedCrossRefGoogle Scholar
  98. 98.
    Ries, J., Yu, S. R., Burkhardt, M., Brand, M., and Schwille, P. (2009) Nat. Methods, 6, 643–645.PubMedCrossRefGoogle Scholar
  99. 99.
    Oehlenschlager, F., Schwille, P., and Eigen, M. (1996) Proc. Natl. Acad. Sci. USA, 93, 12811–12816.PubMedCrossRefGoogle Scholar
  100. 100.
    Walter, N. G., Schwille, P., and Eigen, M. (1996) Proc. Natl. Acad. Sci. USA, 93, 12805–12810.PubMedCrossRefGoogle Scholar
  101. 101.
    Schwille, P., Meyer-Almes, F. J., and Rigler, R. (1997) Biophys. J., 72, 1878–1886.PubMedCrossRefGoogle Scholar
  102. 102.
    Haupts, U., Maiti, S., Schwille, P., and Webb, W. W. (1998) Proc. Natl. Acad. Sci. USA, 95, 13573–13578.PubMedCrossRefGoogle Scholar
  103. 103.
    Persson, G., Thyberg, P., and Widengren, J. (2008) Biophys. J., 94, 977–985.PubMedCrossRefGoogle Scholar
  104. 104.
    Sanden, T., Salomonsson, L., Brzezinski, P., and Widengren, J. (2010) Proc. Natl. Acad. Sci. USA, 107, 4129–4134.PubMedCrossRefGoogle Scholar
  105. 105.
    Magzoub, M., Padmawar, P., Dix, J. A., and Verkman, A. S. (2006) J. Phys. Chem. B, 110, 21216–21221.PubMedCrossRefGoogle Scholar
  106. 106.
    Al Soufi, W., Reija, B., Novo, M., Felekyan, S., Kuhnemuth, R., and Seidel, C. A. (2005) J. Am. Chem. Soc., 127, 8775–8784.CrossRefGoogle Scholar
  107. 107.
    Bonnet, G., Krichevsky, O., and Libchaber, A. (1998) Proc. Natl. Acad. Sci. USA, 95, 8602–8606.PubMedCrossRefGoogle Scholar
  108. 108.
    Kim, H. D., Nienhaus, G. U., Ha, T., Orr, J. W., Williamson, J. R., and Chu, S. (2002) Proc. Natl. Acad. Sci. USA, 99, 4284–4289.PubMedCrossRefGoogle Scholar
  109. 109.
    Shusterman, R., Gavrinyov, T., and Krichevsky, O. (2008) Phys. Rev. Lett., 100, 98–102.CrossRefGoogle Scholar
  110. 110.
    Chattopadhyay, K., Saffarian, S., Elson, E. L., and Frieden, C. (2002) Proc. Natl. Acad. Sci. USA, 99, 14171–14176.PubMedCrossRefGoogle Scholar
  111. 111.
    Neuweiler, H., Johnson, C. M., and Fersht, A. R. (2009) Proc. Natl. Acad. Sci. USA, 106, 18569–18574.PubMedCrossRefGoogle Scholar
  112. 112.
    Dittrich, P. S., and Schwille, P. (2002) Anal. Chem., 74, 4472–4479.PubMedCrossRefGoogle Scholar
  113. 113.
    Kuricheti, K. K., Buschmann, V., and Weston, K. D. (2004) Appl. Spectrosc., 58, 1180–1186.PubMedCrossRefGoogle Scholar
  114. 114.
    Brister, P. C., Kuricheti, K. K., Buschmann, V., and Weston, K. D. (2005) Lab. Chip., 5, 785–791.PubMedCrossRefGoogle Scholar
  115. 115.
    Edel, J. B., and de Mello, A. J. (2003) Anal. Sci., 19, 1065–1069.PubMedCrossRefGoogle Scholar
  116. 116.
    Okagbare, P. I., and Soper, S. A. (2009) Analyst, 134, 97–106.PubMedCrossRefGoogle Scholar
  117. 117.
    Park, H. Y., Qiu, X., Rhoades, E., Korlach, J., Kwok, L. W., Zipfel, W. R., Webb, W. W., and Pollack, L. (2006) Anal. Chem., 78, 4465–4473.PubMedCrossRefGoogle Scholar
  118. 118.
    Van Orden, A., and Keller, R. A. (1998) Anal. Chem., 70, 4463–4471.CrossRefPubMedGoogle Scholar
  119. 119.
    LeCaptain, D. J., and van Orden, A. (2002) Anal. Chem., 74, 1171–1176.PubMedCrossRefGoogle Scholar
  120. 120.
    Bayer, J., and Radler, J. O. (2006) Electrophoresis, 27, 3952–3963.PubMedCrossRefGoogle Scholar
  121. 121.
    Fogarty, K., and van Orden, A. (2009) Methods, 47, 151–158.PubMedCrossRefGoogle Scholar
  122. 122.
    Pan, X., Yu, H., Shi, X., Korzh, V., and Wohland, T. (2007) J. Biomed. Opt., 12, 14–34.Google Scholar
  123. 123.
    Malone, M. H., Sciaky, N., Stalheim, L., Hahn, K. M., Linney, E., and Johnson, G. L. (2007) BMC Biotechnol., 7, 40.PubMedCrossRefGoogle Scholar
  124. 124.
    Van Craenenbroeck, E., Matthys, G., Beirlant, J., and Engelborghs, Y. (1999) J. Fluoresc., 9, 325–331.CrossRefGoogle Scholar
  125. 125.
    Van Craenenbroeck, E., and Engelborghs, Y. (2000) J. Mol. Recognit., 13, 93–100.PubMedCrossRefGoogle Scholar
  126. 126.
    Van Rompaey, E., Sanders, N., de Smedt, S. C., Demeester, J., van Craenenbroeck, E., and Engelborghs, Y. (2000) Macromolecules, 33, 8280–8288.CrossRefGoogle Scholar
  127. 127.
    Van Rompaey, E., Engelborghs, Y., Sanders, N., de Smedt, S. C., and Demeester, J. (2001) Pharm. Res., 18, 928–936.PubMedCrossRefGoogle Scholar
  128. 128.
    Van den Bogaart, G., Mika, J. T., Krasnikov, V., and Poolman, B. (2007) Biophys. J., 93, 154–163.PubMedCrossRefGoogle Scholar
  129. 129.
    Van den Bogaart, G., Kusters, I., Velasquez, J., Mika, J. T., Krasnikov, V., Driessen, A. J., and Poolman, B. (2008) Methods, 46, 123–130.PubMedCrossRefGoogle Scholar
  130. 130.
    Van den Bogaart, G., Guzman, J. V., Mika, J. T., and Poolman, B. (2008) J. Biol. Chem., 283, 33854–33857.PubMedCrossRefGoogle Scholar
  131. 131.
    Pashkovskaya, A., Kotova, E., Zorlu, Y., Dumoulin, F., Ahsen, V., Agapov, I., and Antonenko, Y. (2010) Langmuir, 26, 5726–5733.PubMedCrossRefGoogle Scholar
  132. 132.
    Smith, P. B., Dendramis, K. A., and Chiu, D. T. (2010) Langmuir, 26, 10218–10222.PubMedCrossRefGoogle Scholar
  133. 133.
    Van den Bogaart, G., Krasnikov, V., and Poolman, B. (2007) Biophys. J., 92, 1233–1240.PubMedCrossRefGoogle Scholar
  134. 134.
    Kusters, I., van den Bogaart, G., de Wit, J., Krasnikov, V., Poolman, B., and Driessen, A. (2010) Methods Mol. Biol., 619, 131–143.PubMedCrossRefGoogle Scholar
  135. 135.
    Perevoshchikova, I. V., Zorov, D. B., and Antonenko, Y. N. (2008) Biochim. Biophys. Acta, 1778, 2182–2190.PubMedCrossRefGoogle Scholar
  136. 136.
    Perevoshchikova, I. V., Zorov, S. D., Kotova, E. A., Zorov, D. B., and Antonenko, Y. N. (2010) FEBS Lett., 584, 2397–2402.PubMedCrossRefGoogle Scholar
  137. 137.
    Meyer, T., and Schindler, H. (1988) Biophys. J., 54, 983–993.PubMedCrossRefGoogle Scholar
  138. 138.
    Berland, K. M., So, P. T., Chen, Y., Mantulin, W. W., and Gratton, E. (1996) Biophys. J., 71, 410–420.PubMedCrossRefGoogle Scholar
  139. 139.
    Levi, V., Ruan, Q., Kis-Petikova, K., and Gratton, E. (2003) Biochem. Soc. Trans., 31, 997–1000.PubMedCrossRefGoogle Scholar
  140. 140.
    Lu, H. P. (2005) Acc. Chem. Res., 38, 557–565.PubMedCrossRefGoogle Scholar
  141. 141.
    Novoderezhkin, V. I., Rutkauskas, D., and van Grondelle, R. (2006) Biophys. J., 90, 2890–2902.PubMedCrossRefGoogle Scholar
  142. 142.
    Osad’ko, I. S. (2006) Phys.-Usp., 49, 19–51.CrossRefGoogle Scholar
  143. 143.
    Mukhopadhyay, S., and Deniz, A. A. (2007) J. Fluoresc., 17, 775–783.PubMedCrossRefGoogle Scholar
  144. 144.
    Hilario, J., and Kowalczykowski, S. C. (2010) Curr. Opin. Chem. Biol., 14, 15–22.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • I. V. Perevoshchikova
    • 1
    • 2
  • E. A. Kotova
    • 1
  • Y. N. Antonenko
    • 1
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Department of Biomedical SciencesUniversity of Veterinary MedicineViennaAustria

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