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Biochemistry (Moscow)

, 76:295 | Cite as

IgG-binding proteins of bacteria

  • E. V. SidorinEmail author
  • T. F. Solov’eva
Review

Abstract

Proteins capable of non-immune binding of immunoglobulins G (IgG) of various mammalian species, i.e. without the involvement of the antigen-binding sites of the immunoglobulins, are widespread in bacteria. These proteins are located on the surface of bacterial cells and help them to evade the host’s immune response due to protection against the action of complement and to decrease in phagocytosis. This review summarizes data on the structure of immunoglobulin-binding proteins (IBP) and their complexes with IgG. Common and distinctive structural features of IBPs of gram-positive bacteria (staphylococci, streptococci, peptostreptococci) are discussed. Conditions for IBP expression by bacteria and their functional heterogeneity are considered. Data on IBPs of gram-negative bacteria are presented.

Key words

immunoglobulin G immunoglobulin-binding proteins Fc-fragment of IgG 

Abbreviations

CH

heavy chain constant region domain

Fab

antigen-binding fragment of Ig

Fc

crystallizable fragment of Ig

GAS

group A streptococci

GCS

group C streptococci

GGS

group G streptococci

IBP

immunoglobulin-binding protein

Ig

immunoglobulin

PpL

peptostreptococcal protein L

PsaA

pH-6 antigen

Sbi

second IBP of staphylococci

Sib

second IBP of group A streptococci

Skp

chaperon protein

SpA

staphylococcal protein A

SpG

protein G of group C and G streptococci

SSL

staphylococcal superantigen-like protein

VH

heavy chain variable region domain

VL

light chain variable region domain

References

  1. 1.
    Kihlberg, B.-M., Collin, M., Olsen, A., and Bjorck, L. (1999) Infect. Immun., 67, 1708–1714.PubMedGoogle Scholar
  2. 2.
    Tolo, K., and Helgeland, K. (1991) Oral. Microbiol. Immunol., 6, 373–377.PubMedGoogle Scholar
  3. 3.
    Widders, P. R., Dorrance, L. A., Yarnall, M., and Corbeil, L. B. (1989) Infect. Immun., 57, 639–342.PubMedGoogle Scholar
  4. 4.
    Bjorck, L. (1988) J. Immunol., 140, 1194–1197.PubMedGoogle Scholar
  5. 5.
    Raeder, R., Faulmann, E. L., and Boyle, M. D. (1991) J. Immunol., 146, 1247–1253.PubMedGoogle Scholar
  6. 6.
    Labbe, S., and Grenier, D. (1995) Infect. Immun., 63, 2785–2789.PubMedGoogle Scholar
  7. 7.
    Bjorck, L., and Kronvall, G. (1984) J. Immunol., 133, 969–974.PubMedGoogle Scholar
  8. 8.
    Akesson, P., Schmidt, K. H., Cooney J., and Bjorck, L. (1994) Biochem. J., 300, 877–886.PubMedGoogle Scholar
  9. 9.
    Yarnall, M., Widders, P. R., and Corbeil, L. B. (1988) Scand. J. Immunol., 28, 129–137.PubMedGoogle Scholar
  10. 10.
    Yarnall, M., and Widders, P. R. (1989) J. Med. Microbiol., 28, 137–141.PubMedGoogle Scholar
  11. 11.
    Mintz, K. P., and Fivestaylor, P. M. (1994) Infec. Immun., 62, 4500–4505.Google Scholar
  12. 12.
    Zavyalov, V. P., Abramov, V. M., Cherepanov, P. G., Spirina, G. V., Chernovskaya, T. V., Vasiliev, N. P., and Zavyalova, G. A. (1996) FEMS Immunol. Med. Microb., 14, 53–57.Google Scholar
  13. 13.
    Sandt, C. H., Wang, Y.-D., Wilson, R. A., and Hill, C. W. (1997) Infect. Immun., 65, 4572–4579.PubMedGoogle Scholar
  14. 14.
    Yarnall, M., Reis, K. J., Ayoub, E. M., and Boyle, M. D. P. (1984) J. Microbiol. Meth., 3, 83–93.Google Scholar
  15. 15.
    Reis, K. J., Siden, E. J., and Boyle, M. D. P. (1988) Biotechniques, 6, 130–136.PubMedGoogle Scholar
  16. 16.
    Kawabata, S., Tamura, Y., Murakami, J., Terao, Y., Nakagawa, I., and Hamada, S. (2002) Biochem. Biophys. Res. Commun., 296, 1329–1333.PubMedGoogle Scholar
  17. 17.
    Akerstrom, B., Brodin, T., Reis, K., and Bjorck, L. (1985) J. Immunol., 135, 2589–2592.PubMedGoogle Scholar
  18. 18.
    Sjobring, U., Trojnar, J., Grubb, A., Akerstrom, B., and Bjorck, L. (1989) J. Immunol., 143, 2948–2954.PubMedGoogle Scholar
  19. 19.
    Jonsson, H., Burtsoff-Asp, C., and Guss, B. (1995) Biochim. Biophys. Acta, 1249, 65–71.PubMedGoogle Scholar
  20. 20.
    Patella, V., Casolaro, V., Bjorck, L., and Marone, G. (1990) J. Immunol., 145, 3054–3061.PubMedGoogle Scholar
  21. 21.
    Boyle, M. D. P., and Reis, K. J. (1987) Biotechnology, 5, 697–703.Google Scholar
  22. 22.
    Boyle, M. D. P. (1990) in Bacterial Immunoglobulin-Binding Proteins. Applications in Immunotechnology, Vol. 2 (Boyle, M., ed.) Academic Press, Inc., San Diego, pp. 3–13.Google Scholar
  23. 23.
    Boyle, M. D. P. (1998) Encyclopedia of Immunology, 2nd Edn., Academic Press, N. Y., pp. 323–327.Google Scholar
  24. 24.
    Cunningham, M. W. (2000) Clin. Microbiol., 13, 470–511.Google Scholar
  25. 25.
    Navarre, W. W., and Schneewind, O. (1999) Microbiol. Mol. Biol., 63, 174–229.Google Scholar
  26. 26.
    Kazeeva, T. N., and Shevelev, A. B. (2009) Biochemistry (Moscow), 74, 12–21.Google Scholar
  27. 27.
    Myhre, E. B., and Kronvall, G. (1977) Infect. Immun., 17, 475–482.PubMedGoogle Scholar
  28. 28.
    Frick, I. M., Wikstrm, M., Forsen, S., Drakenberg, T., Gomi, H., Sjobring, U., and Bjorck, L. (1992) Proc. Natl. Acad. Sci. USA, 89, 8532–8536.PubMedGoogle Scholar
  29. 29.
    Gouda, H., Torigoe, H., Saito, A., Sato, M., Arata, Y., and Schimada, I. (1992) Biochemistry, 31, 9665–9672.PubMedGoogle Scholar
  30. 30.
    Derrick, J. P., and Wigley, D. B. (1992) Nature, 359, 752–754.PubMedGoogle Scholar
  31. 31.
    Starovasnik, M. A., O’Connell, M. P., Fairbrother, W. J., and Kelley, R. F. (1999) Protein Sci., 8, 1423–1431.PubMedGoogle Scholar
  32. 32.
    Lian, L.-Y., Barsukov, I. L., Derrick, J. P., and Roberts, G. C. K. (1994) Nat. Struct. Biol., 1, 355–357.PubMedGoogle Scholar
  33. 33.
    Fischetti, V. A., Pancholi, V., and Schneewind, O. (1990) Mol. Microbiol., 4, 1603–1605.PubMedGoogle Scholar
  34. 34.
    Ton-That, H., Labischinski, H., Berger-Bachi, B., and Schneewind, O. J. (1998) Biol. Chem., 273, 29143–29149.Google Scholar
  35. 35.
    Schneewind, O., Model, P., and Fischetti, V. A. (1992) Cell, 70, 267–281.PubMedGoogle Scholar
  36. 36.
    Bucin, D., Johansson, S., Malm, T., Jogi, P., Johansson, J., Westrin, P., Lindberg, L. O., Olsson, A. K., Gelberg, J., Peres, V., Harling, S., Bennhagen, R., Kornhall, B., Ekmehag, B., Kurkus, J., and Otto, G. (2006) Transpl. Int., 19, 239–244.PubMedGoogle Scholar
  37. 37.
    Haas, M., Bohmig, G. A., Leko-Mohr, Z., Exner, M., Regele, H., Derfler, K., Horl, W. H., and Druml, W. (2002) Nephrol. Dial. Transplant., 17, 1503–1508.PubMedGoogle Scholar
  38. 38.
    Josic, D., and Lim, Y.-P. (2001) Food Technol. Biotechnol., 39, 215–226.Google Scholar
  39. 39.
    Jensen, K. (1958) Acta Pathol. Microbiol. Scand., 44, 421–428.Google Scholar
  40. 40.
    Forsgren, A., and Sjoquist, J. (1966) J. Immunol., 97, 822–827.PubMedGoogle Scholar
  41. 41.
    Lind, I., Reyn, A., and Birch-Anderson, A. (1972) Acta Path. Microbiol. Scand., 80, 281–291.Google Scholar
  42. 42.
    Forsgren, A. (1970) Infect. Immun., 2, 672–673.PubMedGoogle Scholar
  43. 43.
    Bjork, I., Petersson, B. A., and Sjoquist, J. (1972) Eur. J. Biochem., 29, 579–584.PubMedGoogle Scholar
  44. 44.
    Lindmark, R., Movitz, J., and Sjoquist, J. (1977) Eur. J. Biochem., 74, 623–628.PubMedGoogle Scholar
  45. 45.
    Dossett, J. H., Kronvall, G., Williams, R. C., and Quie, P. G. (1969) J. Immunol., 103, 1405–1410.Google Scholar
  46. 46.
    Lind, I. (1974) Acta Pathol. Microbiol. Scand., 82, 821–828.Google Scholar
  47. 47.
    Winblad, S., and Ericson, C. (1973) Acta Pathol. Microbiol. Scand., 81, 150–156.Google Scholar
  48. 48.
    Lind, I. (1972) Acta Pathol. Microbiol. Scand., 80, 702–708.Google Scholar
  49. 49.
    Cohen, S., and Sweeney, H. M. (1979) J. Bacteriol., 140, 1028–1035.PubMedGoogle Scholar
  50. 50.
    Cheung, A. L., Bayer, A. S., Peters, J., and Ward, J. I. (1987) Infect. Immun., 55, 843–847.PubMedGoogle Scholar
  51. 51.
    Lofkvist, T., and Sjoquist, J. (1962) Acta Pathol. Microbiol. Scand., 56, 295–304.Google Scholar
  52. 52.
    Sjoholm, I. (1975) Eur. J. Biochem., 51, 55–61.PubMedGoogle Scholar
  53. 53.
    Abrahmsen, L., Moks, T., Nilsson, B., Hellman, U., and Uhlen, M. (1985) EMBO J., 4, 3901–3906.PubMedGoogle Scholar
  54. 54.
    Moks, T., Abrahmsen, L., Nilsson, B., Hellman, U., Sjoquist, J., and Uhlen, M. (1986) Eur. J. Biochem., 156, 637–643.PubMedGoogle Scholar
  55. 55.
    Sjodahl, J. (1977) Eur. J. Biochem., 73, 343–351.PubMedGoogle Scholar
  56. 56.
    Guss, B., Uhlen, M., Nilsson, B., Lindberg, M., Sjoquist, J., and Sjodahl, J. (1984) Eur. J. Biochem., 138, 413–420.PubMedGoogle Scholar
  57. 57.
    Schneewind, O., Fowler, A., and Faull, K. F. (1995) Science, 268, 103–106.PubMedGoogle Scholar
  58. 58.
    Brigido, M. D. M., Barardi, C. R., Bonjardin, C. A., Santos, C. L., Junqueira, M. L., and Brentani, R. R. (1991) J. Basic Microbiol., 31, 337–345.Google Scholar
  59. 59.
    Upadhyay, A., Burman, J. D., Clark, E. A., Leung, E., Isenman, D. E., van den Elsen, J. M. H., and Bagby, S. (2008) J. Biol. Chem., 283, 22113–22120.PubMedGoogle Scholar
  60. 60.
    Frick, I. M., Akesson, P., Cooney, J., Sjobring, U., Schmidt, K. H., Gomi, H., Hattori, S., Tagawa, C., Kishimoto, F., and Bjorck, L. (1994) Mol. Microbiol., 12, 143–151.PubMedGoogle Scholar
  61. 61.
    Frick, I. M., Crossin, K. L., Edelman, G. M., and Bjorck, L. (1995) EMBO J., 14, 1674–1679.PubMedGoogle Scholar
  62. 62.
    Olsson, A., Eliasson, M., Guss, B., Nilsson, B., Hellman, U., Lindberg, M., and Uhlen, M. (1987) Eur. J. Biochem., 168, 319–324.PubMedGoogle Scholar
  63. 63.
    Kastern, W., Sjobring, U., and Bjorck, L. (1992) J. Biol. Chem., 267, 12820–12825.PubMedGoogle Scholar
  64. 64.
    Murphy, J. P., Trowern, A. R., and Duggleby, C. J. (1994) DNA Seq., 4, 259–265.PubMedGoogle Scholar
  65. 65.
    Akerstrom, B., and Bjorck, L. (1986) J. Biol. Chem., 261, 10240–10247.PubMedGoogle Scholar
  66. 66.
    Akerstrom, P., Cooney, J., Kishimoto, F., and Bjorck, L. (1990) Mol. Immunol., 27, 523–531.Google Scholar
  67. 67.
    Akerstrom, B., and Bjorck, L. (1989) J. Biol. Chem., 264, 19740–19746.PubMedGoogle Scholar
  68. 68.
    Axcrona, K., Bjorck, L., and Leanderson, T. (1995) Scand. J. Immunol., 42, 359–367.PubMedGoogle Scholar
  69. 69.
    Forsgren, A. (1968) J. Immunol., 100, 927–930.PubMedGoogle Scholar
  70. 70.
    Kronvall, G., Grey, H. M., and Williams, R. C. (1970) J. Immunol., 105, 1116–1123.PubMedGoogle Scholar
  71. 71.
    Jansson, B., Uhlen, M., and Nygren, P. A. (1998) FEMS Immunol. Med. Microbiol., 20, 69–78.PubMedGoogle Scholar
  72. 72.
    Jacobsson, K., and Frykberg, L. (1995) Biotechniques, 18, 878–885.PubMedGoogle Scholar
  73. 73.
    Zhang, L., Jacobsson, K., Vasi, J., Lindberg, M., and Frykberg, L. (1998) Microbiology, 144, 985–991.PubMedGoogle Scholar
  74. 74.
    Atkins, K. L., Burman, J. D., Chamberlain, E. S., Cooper, J. E., Poutrel, B., Bagby, S., Jenkins, A. T. A., Feil, E. J., and van den Elsen, J. M. H. (2008) Mol. Immunol., 45, 1600–1611.PubMedGoogle Scholar
  75. 75.
    Deisenhofer, J., Jones, T. A., Huber, R., Sjodahl, J., and Sjoquist, J. (1978) Hoppe Seylers Z. Physiol. Chem., 359, 975–985.PubMedGoogle Scholar
  76. 76.
    Burman, J. D., Leung, E., Atkins, K. L., O’sheaghdha, M. N., Lango, L., Bernardo, P., Bagby, S., Svergun, D. I., Foster, T. J., Isenman, D. E., and van den Elsen, J. M. H. (2008) J. Biol. Chem., 283, 17579–17593.PubMedGoogle Scholar
  77. 77.
    Clark, E., Upadhyay, A., Bagby, S., and van den Elsen, J. (2009) Mol. Immunol., 46, 2834–2835.Google Scholar
  78. 78.
    Itoh, S., Hamada, E., Kamoshida, G., Yokoyama, R., Takii, T., Onozaki, K., and Tsuji, T. (2010) Mol. Immunol., 47, 932–938.PubMedGoogle Scholar
  79. 79.
    Ramsland, P. A., Willoughby, N., Trist, Y. V., Farrugia, W., Hogarth, P. M., Fraser, J. D., and Wines, B. D. (2007) Proc. Natl. Acad. Sci. USA, 104, 15051–15056.PubMedGoogle Scholar
  80. 80.
    Bessen, D. E., and Fischetti, V. A. (1992) Infect. Immun., 60, 124–135.PubMedGoogle Scholar
  81. 81.
    Podbielski, A., Schnitzler, N., Beyhs, P., and Boyle, M. D. (1996) Mol. Microbiol., 19, 429–441.PubMedGoogle Scholar
  82. 82.
    Thern, A., Wastfelt, M., and Lindahl, G. (1998) J. Immunol., 160, 860–869.PubMedGoogle Scholar
  83. 83.
    Phillips, G. N., Flicker, P. F., Cohen, C., Manjula, B. N., and Fischetti, V. A. (1981) Proc. Natl. Acad. Sci. USA, 78, 4693–4698.Google Scholar
  84. 84.
    Fischetti, V. A. (1989) Clin. Microbiol., 2, 285–314.Google Scholar
  85. 85.
    Hollingshead, S. K., Fischetti, V. A., and Scott, J. R. (1987) Infect. Immun., 55, 3237–3239.PubMedGoogle Scholar
  86. 86.
    Cunningham, M. W. (2000) Clin. Microbiol., 13, 470–511.Google Scholar
  87. 87.
    Akerstrom, B., Lindqvist, A., and Lindahl, G. (1991) Mol. Immunol., 28, 349–357.PubMedGoogle Scholar
  88. 88.
    Heden, L. O., and Lindahl, G. (1993) J. Gen. Microbiol., 139, 2067–2074.PubMedGoogle Scholar
  89. 89.
    Stenberg, L., O’Toole, P., and Lindahl, G. (1992) Mol. Microbiol., 6, 1185–1194.PubMedGoogle Scholar
  90. 90.
    Boyle, M. D., Weber-Heynemann, J., Raeder, R., and Podbielski, A. (1995) Mol. Immunol., 32, 669–678.PubMedGoogle Scholar
  91. 91.
    Schmidt, K. H., and Wadstrom, T. (1990) Zentralbl. Bakteriol., 273, 216–228.PubMedGoogle Scholar
  92. 92.
    Benghezal, M., Lipke, P. N., and Conzelmann, A. (1995) J. Cell Biol., 130, 1333–1344.PubMedGoogle Scholar
  93. 93.
    Johnsson, E., Thern, A., Dahlback, B., Heden, L. O., Wikstrom, M., and Lindahl, G. (1996) J. Immunol., 157, 3021–3029.PubMedGoogle Scholar
  94. 94.
    Thern, A., Stenberg, L., Dahlback, B., and Lindahl, G. (1995) J. Immunol., 154, 375–386.PubMedGoogle Scholar
  95. 95.
    Boyle, M. D., Hawlitzky, J., Raeder, R., and Podbielski, A. (1994) Infect. Immun., 62, 1336–1347.PubMedGoogle Scholar
  96. 96.
    Fagan, K. P., Reinscheid, D., Gottschalk, B., and Chhatwal, G. S. (2001) Infect. Immun., 69, 4851–4857.PubMedGoogle Scholar
  97. 97.
    Reis, K. J., Ayoub, E. M., and Boyle, M. D. (1984) J. Immunol., 132, 3091–3097.PubMedGoogle Scholar
  98. 98.
    Reis, K. J., Ayoub, E. M., and Boyle, M. D. (1984) J. Immunol., 132, 3098–3102.PubMedGoogle Scholar
  99. 99.
    Sjobring, U., Falkenberg, C., Nielsen, E., Akerstrom, B., and Bjorck, L. (1988) J. Immunol., 140, 1595–1599.PubMedGoogle Scholar
  100. 100.
    Guss, B., Eliasson, M., Olsson, A., Uhlen, M., Frej, A. K., Jornvall, H., Flock, J. I., and Lindberg, M. (1986) EMBO J., 5, 1567–1575.PubMedGoogle Scholar
  101. 101.
    Filpula, D., Alexander, P., and Fahnestock, S. R. (1987) Nucleic Acids Res., 15, 7210.PubMedGoogle Scholar
  102. 102.
    Fahnestock, S. R., Alexander, P., Nagle, J., and Filpula, D. (1986) J. Bacteriol., 167, 870–880.PubMedGoogle Scholar
  103. 103.
    Sjobring, U., Bjorck, L., and Kastern, W. (1991) J. Biol. Chem., 266, 399–405.PubMedGoogle Scholar
  104. 104.
    Bjorck, L., Kastern, W., Lindahl, G., and Wideback, K. (1987) Mol. Immunol., 24, 1113–1122.PubMedGoogle Scholar
  105. 105.
    Johansson, M. U., de Chateau, M., Wikstrom, M., Forsen, S., Drakenberg, T., and Bjorck, L. (1997) J. Mol. Biol., 266, 859–865.PubMedGoogle Scholar
  106. 106.
    Sjobring, U., Bjorck, L., and Kastern, W. (1989) Mol. Microbiol., 3, 319–327.PubMedGoogle Scholar
  107. 107.
    Gallagher, T., Alexander, P., Bryan, P., and Gilliland, G. L. (1994) Biochemistry, 33, 4721–4729.PubMedGoogle Scholar
  108. 108.
    Achari, A., Hale, S. P., Howard, A. J., Clore, G. M., Gronenborn, A. M., Hardman, K. D., and Whitlow, M. (1992) Biochemistry, 31, 10449–10457.PubMedGoogle Scholar
  109. 109.
    Derrick, J. P., and Wigley, D. B. (1994) J. Mol. Biol., 243, 906–918.PubMedGoogle Scholar
  110. 110.
    Sauer-Eriksson, A. E., Kleywegt, G. J., Uhlen, M., and Jones, T. A. (1995) Structure, 3, 265–278.PubMedGoogle Scholar
  111. 111.
    Jonsson, H., Frykberg, L., Rantamaki, L., and Guss, B. (1994) Gene, 143, 85–89.PubMedGoogle Scholar
  112. 112.
    Jonsson, H., and Muller, H. P. (1994) Eur. J. Biochem., 220, 819–826.PubMedGoogle Scholar
  113. 113.
    Jonsson, H., Lindmark, H., and Guss, B. (1995) Infect. Immun., 63, 2968–2975.PubMedGoogle Scholar
  114. 114.
    Nitsche-Schmitz, D. P., Johansson, H. M., Sastalla, I., Reissmann, S., Frick, I.-M., and Chhatwal, G. S. (2007) J. Biol. Chem., 282, 17530–17536.PubMedGoogle Scholar
  115. 115.
    Vasi, J., Frykberg, L., Carlsson, L. E., Lindberg, M., and Guss, B. (2000) Infect. Immun., 68, 294–302.PubMedGoogle Scholar
  116. 116.
    Meehan, M., Lynagh, Y., Woods, C., and Owen, P. (2001) Microbiology, 147, 3311–3332.PubMedGoogle Scholar
  117. 117.
    Enokizono, J., Wikstrom, M., Sjobring, U., Bjorck, L., Forsen, S., Arata, Y., Kato, K., and Shimada, I. (1997) J. Mol. Biol., 270, 8–13.PubMedGoogle Scholar
  118. 118.
    Nilson, B. H., Solomon, A., Bjorck, L., and Akerstrom, B. (1992) J. Biol. Chem., 267, 2234–2239.PubMedGoogle Scholar
  119. 119.
    Wikstrom, M., Sjobring, U., Drakenberg, T., Forsen, S., and Bjorck, L. (1995) J. Mol. Biol., 250, 128–133.PubMedGoogle Scholar
  120. 120.
    Murphy, J. P., Duggleby, C. J., Atkinson, M. A., Trowen, A. R., Atkinson, T., and Goward, C. R. (1994) Mol. Microbiol., 12, 911–920.PubMedGoogle Scholar
  121. 121.
    Wikstrom, M., Drakenberg, T., Forsen, S., Sjobring, U., and Bjorck, L. (1994) Biochemistry, 33, 14011–14017.PubMedGoogle Scholar
  122. 122.
    Wikstrom, M., Sjobring, U., Kastern, W., Bjorck, L., Drakenberg, T., and Forsen, S. (1993) Biochemistry, 32, 3381–3386.PubMedGoogle Scholar
  123. 123.
    Bottomley, S. P., Beckingham, J. A., Murphy, J. P., Atkinson, M., Atkinson, T., Hinton, R. J., and Gore, M. G. (1995) Bioseparation, 5, 359–367.PubMedGoogle Scholar
  124. 124.
    Gu, H. D., Yi, Q. A., Bray, S. T., Riddle, D. S., Shiau, A. K., and Baker, D. (1995) Protein Sci., 4, 1108–1117.PubMedGoogle Scholar
  125. 125.
    Demuth, D. R., Davis, C. A., Corner, A. M., Lamont, R. J., Leboy, P. S., and Malamud, D. (1988) Infect. Immun., 56, 2484–2490.PubMedGoogle Scholar
  126. 126.
    Lewis, M. J., Meehan, M., Owen, P., and Woof, J. M. (2008) J. Biol. Chem., 283, 17615–17623.PubMedGoogle Scholar
  127. 127.
    Deisenhofer, J. (1981) Biochemistry, 20, 2361–2370.PubMedGoogle Scholar
  128. 128.
    Lewis, M., Wagner, B., and Woof, J. M. (2008) Mol. Immunol., 45, 818–827.PubMedGoogle Scholar
  129. 129.
    Graille, M., Stura, E. A., Corper, A. L., Sutton, B. J., Taussig, M. J., Charbonnier, J.-B., and Silverman, G. J. (2000) Proc. Natl. Acad. Sci. USA, 97, 5399–5404.PubMedGoogle Scholar
  130. 130.
    Graille, M., Stura, E. A., Housden, N. G., Beckingham, J. A., Bottomley, S. P., Beale, D., Taussig, M. J., Sutton, B. J., Gore, M. G., and Charbonnier, J. B. (2001) Structure, 9, 679–687.PubMedGoogle Scholar
  131. 131.
    Graille, M., Harrison, S., Crump, M. P., Findlow, S. C., Housden, N. G., Muller, B. H., Battail-Poirot, N., Sibai, G., Sutton, B. J., Taussig, M. J., Jolivet-Reynaud, C., Gore, M. G., and Stura, E. A. (2002) J. Biol. Chem., 277, 47500–47506.PubMedGoogle Scholar
  132. 132.
    Reza, A. H., Ascencio, F., Ljungh, A., and Wadstrom, T.(1995) Zentralbl. Bakteriol., 282, 255–264.PubMedGoogle Scholar
  133. 133.
    Corbeil, L. B., Bastida-Corcuera, F. D., and Beveridge, T. J. (1997) Infect. Immun., 65, 4250–4257.PubMedGoogle Scholar
  134. 134.
    Linder, L. L., Klempner, M. S., and Straley, S. C. (1990) Infect. Immun., 58, 2569–2577.Google Scholar
  135. 135.
    Makoveichuk, E., Cherepanov, P., Lundberg, S., Forsberg, A., and Olivecrona, G. (2003) J. Lipid Res., 44, 320–330.PubMedGoogle Scholar
  136. 136.
    Sidorin, E. V., Kim, N. Yu., Leichenko, E. V., Anastyuk, S. D., Dmitrenok, P. S., Naberezhnykh, G. A., and Solov’eva, T. F. (2006) Biochemistry (Moscow), 71, 1278–1283.Google Scholar
  137. 137.
    Sidorin, E. V., Ziganshin, R. Kh., Naberezhnykh, G. A., Likhatskaya, G. N., Trifonov, E. V., Anastyuk, S. D., Chernikov, O. V., and Solov’eva, T. F. (2009) Biochemistry (Moscow), 74, 406–415.Google Scholar
  138. 138.
    Meininger, D. P., Rance, M., Starovasnik, A., Fairbrother, W. J., and Skelton, N. J. (2000) Biochemistry, 39, 26–36.PubMedGoogle Scholar
  139. 139.
    Sandt, C. H., and Hill, C. W. (2000) Infect. Immun., 68, 2205–2214.PubMedGoogle Scholar
  140. 140.
    Sandt, C. H., and Hill, C. W. (2001) Infect. Immun., 69, 7293–7303.PubMedGoogle Scholar
  141. 141.
    Lu, Y., Iyoda, S., Satou, H., Satou, H., Itoh, K., Saitoh, T., and Watanabe, H. (2006) Infect. Immun., 74, 5747–5755.PubMedGoogle Scholar
  142. 142.
    Leo, J. C., and Goldman, A. (2009) Mol. Immunol., 46, 1860–1866.PubMedGoogle Scholar
  143. 143.
    Leo, J. C., and Goldman, A. (2010) Mol. Immunol., 47, 1870–1872.PubMedGoogle Scholar
  144. 144.
    Guo, M., Han, Y. W., Sharma, A., and de Nardin, E. (2000) Oral. Microbiol. Immunol., 15, 119–123.PubMedGoogle Scholar
  145. 145.
    Bastida-Corcuera, F. D., Nielsen, K. H., and Corbeil, L. B. (1999) Vet. Immunol. Immunopathol., 71, 143–149.PubMedGoogle Scholar
  146. 146.
    Yang, Y., and Isberg, R. R. (1997) Mol. Microb., 24, 499–510.Google Scholar
  147. 147.
    Naberezhnykh, G. A., Sidorin, E. V., Lapshina, L. A., Reunov, A. V., and Solov’eva, T. F. (2006) Biochemistry (Moscow), 71, 1284–1288.Google Scholar
  148. 148.
    Widders, P. R., Smith, J. W., Yarnall, M., McGuire, T. C., and Corbeil, L. B. (1988) J. Med. Microbiol., 26, 307–311.PubMedGoogle Scholar
  149. 149.
    Grover, S., McGee, Z. A., and Odell, W. D. (1991) J. Immunol. Meth., 141, 187–197.Google Scholar
  150. 150.
    Amini, H.-R., Ascencio, F., Cruz-Villacorta, A., Ruiz-Bustos, E., and Wadstrom, T. (1996) FEMS Immunol. Med. Microbiol., 16, 163–172.PubMedGoogle Scholar
  151. 151.
    Levinson, A. I., Kozlowski, L., Zheng, Y., and Wheatley, L. (1995) J. Clin. Immunol., 15, 26S–36S.PubMedGoogle Scholar
  152. 152.
    Burova, L. A., and Totolyan, A. A. (1988) Revmatologiya, 3, 9–12.Google Scholar
  153. 153.
    Burova, L. A., Pigarevsky, P. V., Gladilina, M. M., Nagornev, V. A., and Totolyan, A. A. (2001) Med. Immunol. (Moscow), 3, 213–214.Google Scholar
  154. 154.
    Kihlberg, B.-M., Sjoholm, A. G., Bjorck, L., and Sjobring, U. (1996) Eur. J. Biochem., 240, 556–563.PubMedGoogle Scholar
  155. 155.
    Eliasson, M., Olsson, A., Palmcrantz, E., Wiberg, K., Inganas, M., Guss, B., Lindberg, M., and Uhlen, M. (1988) J. Biol. Chem., 263, 4323–4327.PubMedGoogle Scholar
  156. 156.
    Jiang, S. H., Wang, J. F., Xu, R., Liu, Y. J., Wang, X. N., Cao, J., Zhao, P., Shen, Y. J., Yang, T., Yang, H., Jia, J. A., Chen, Q. L., and Pan, W. (2008) DNA Cell Biol., 27, 423–431.PubMedGoogle Scholar
  157. 157.
    Svensson, H. G., Hoogenboom, H. R., and Sjobring, U. (1998) Eur. J. Biochem., 258, 890–896.PubMedGoogle Scholar

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© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  1. 1.Pacific Institute of Bioorganic ChemistryFar-Eastern Division of the Russian Academy of SciencesVladivostokRussia

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