Pseudomonas Aeruginosa Lectins As Targets for Novel Antibacterials

Cover Page

Abstract


Pseudomonas aeruginosa is one of the most widespread and troublesome opportunistic pathogens that is capable of colonizing various human tissues and organs and is often resistant to many currently used antibiotics. This resistance is caused by different factors, including the acquisition of specific resistance genes, intrinsic capability to diminish antibiotic penetration into the bacterial cell, and the ability to form biofilms. This situation has prompted the development of novel compounds differing in their mechanism of action from traditional antibiotics that suppress the growth of microorganisms or directly kill bacteria. Instead, these new compounds should decrease the pathogens’ ability to colonize and damage human tissues by inhibiting the virulence factors and biofilm formation. The lectins LecA and LecB that bind galactose and fucose, as well as oligo- and polysaccharides containing these sugars, are among the most thoroughly-studied targets for such novel antibacterials. In this review, we summarize the results of experiments highlighting the importance of these proteins for P. aeruginosa pathogenicity and provide information on existing lectins inhibitors and their effectiveness in various experimental models. Particular attention is paid to the effects of lectins inhibition in animal models of infection and in clinical practice. We argue that lectins inhibition is a perspective approach to combating P. aeruginosa. However, despite the existence of highly effective in vitro inhibitors, further experiments are required in order to advance these inhibitors into pre-clinical studies.


A. V. Grishin

Gamaleya Research Center of Epidemiology and Microbiology; Institute of Agricultural Biotechnology

Author for correspondence.
Email: grishin-a1@yandex.ru

Russian Federation

M. S. Krivozubov

Gamaleya Research Center of Epidemiology and Microbiology

Email: grishin-a1@yandex.ru

Russian Federation

A. S. Karyagina

Gamaleya Research Center of Epidemiology and Microbiology; Institute of Agricultural Biotechnology; Lomonosov Moscow State University

Email: grishin-a1@yandex.ru

Russian Federation

A. L. Gintsburg

Gamaleya Research Center of Epidemiology and Microbiology

Email: grishin-a1@yandex.ru

Russian Federation

  1. Blanc D.S., Petignat C., Janin B., Bille J., Francioli P. // Clin. Microbiol. Infect. 1998, V.4, №5, P.242-247
  2. Mesaros N., Nordmann P., Plésiat P., Roussel-Delvallez M., van Eldere J., Glupczynski Y., van Laethem Y., Jacobs F., Lebecque P., Malfroot A. // Clin. Microbiol. Infect. 2007, V.13, №6, P.560-578
  3. Donlan R.M., Costerton J.W. // Clin. Microbiol. Rev. 2002, V.15, №2, P.167-193
  4. Hall-Stoodley L., Costerton J.W., Stoodley P. // Nat. Rev. Microbiol. 2004, V.2, №2, P.95-108
  5. Costerton J.W. // Science. 1999, V.284, №5418, P.1318-1322
  6. Clatworthy A.E., Pierson E., Hung D.T. // Nat. Chem. Biol. 2007, V.3, №9, P.541-548
  7. Gilboa-Garber N. // FEBS Lett. 1972, V.20, №2, P.242-244
  8. Gilboa-Garber N., Mizrahi L., Garber N. // Can. J. Biochem. 1977, V.55, №9, P.975-981
  9. Gilboa-Garber N. // Methods Enzymol. 1982, V.83, №1980, P.378-385
  10. Avichezer D., Katcoff D.J., Garber N.C., Gilboa-Garber N. // J. Biol. Chem. 1992, V.267, №32, P.23023-23027
  11. Gilboa-Garber N., Katkoff D.J., Garber N.C. // FEMS Immunol. Med. Microbiol. 2000, V.29, P.53-57
  12. Cioci G., Mitchell E.P., Gautier C., Wimmerová M., Sudakevitz D., Pérez S., Gilboa-Garber N., Imberty A. // FEBS Lett. 2003, V.555, №2, P.297-301
  13. Mitchell E., Houles C., Sudakevitz D., Wimmerova M., Gautier C., Pérez S., Wu A.M., Gilboa-Garber N., Imberty A. // Nat. Struct. Biol. 2002, V.9, №12, P.918-921
  14. Winzer K., Falconer C., Garber N.C., Diggle S.P., Camara M., Williams P. // Journal of Bacteriology 2000, V.182, №22, P.6401-6411
  15. Diggle S.P., Winzer K., Chhabra S.R., Worrall K.E., Cámara M., Williams P. // Mol. Microbiol. 2003, V.50, №1, P.29-43
  16. Bjarnsholt T., Tolker-Nielsen T., Høiby N., Givskov M. // Expert Rev. Mol. Med. 2010, V.12, P.e11
  17. Pessi G., Williams F., Hindle Z., Heurlier K., Holden M.T., Cámara M., Haas D., Williams P. // Journal of Bacteriology 2001, V.183, №22, P.6676-6683
  18. Diggle S.P., Winzer K., Lazdunski A., Williams P., Camara M. // Journal of Bacteriology 2002, V.184, №10, P.2576-2586
  19. Wu L., Estrada O., Zaborina O., Bains M., Shen L., Kohler J.E., Patel N., Musch M.W., Chang E.B., Fu Y.X. // Science. 2005, V.309, №5735, P.774-777
  20. Kipnis E., Sawa T., Wiener-Kronish J. // Médecine Mal. Infect. 2006, V.36, №2, P.78-91
  21. Alverdy J., Holbrook C., Rocha F., Seiden L., Wu R.L., Musch M., Chang E., Ohman D., Suh S. // Ann. Surg. 2000, V.232, №4, P.480-489
  22. Kohler J.E., Zaborina O., Wu L., Wang Y., Bethel C., Chen Y., Shapiro J., Turner J.R., Alverdy J.C. // Am. J. Physiol. Gastrointest. Liver Physiol. 2005, V.288, №5, P.G1048-G1054
  23. Zaborina O., Lepine F., Xiao G., Valuckaite V., Chen Y., Li T., Ciancio M., Zaborin A., Petrof E.O., Petroff E. // PLoS Pathog. 2007, V.3, №3, P.e35
  24. Glick J., Garber N. // J. Gen. Microbiol. 1983, V.129, №10, P.3085-3090
  25. Tielker D., Hacker S., Loris R., Strathmann M., Wingender J., Wilhelm S., Rosenau F., Jaeger K.E. // Microbiology. 2005, V.151, Pt5, P.1313-1323
  26. Funken H., Bartels K.M., Wilhelm S., Brocker M., Bott M., Bains M., Hancock R.E.W., Rosenau F., Jaeger K.E. // PLoS One. 2012, V.7, №10, P.e46857
  27. Fito-Boncompte L., Chapalain A., Bouffartigues E., Chaker H., Lesouhaitier O., Gicquel G., Bazire A., Madi A., Connil N., Véron W. // Infect. Immun. 2011, V.79, №3, P.1176-1186
  28. Gilboa-Garber N., Sudakevitz D., Sheffi M., Sela R., Levene C. // Glycoconj. J. 1994, V.11, №5, P.414-417
  29. Lanne B., Cîopraga J., Bergström J., Motas C., Karlsson K.A. // Glycoconj. J. 1994, V.11, №4, P.292-298
  30. Chen C.P., Song S.C., Gilboa-Garber N., Chang K.S., Wu A.M. // Glycobiology. 1998, V.8, №1, P.7-16
  31. Blanchard B., Nurisso A., Hollville E., Tétaud C., Wiels J., Pokorná M., Wimmerová M., Varrot A., Imberty A. // J. Mol. Biol. 2008, V.383, №4, P.837-853
  32. Perret S., Sabin C., Dumon C., Pokorná M., Gautier C., Galanina O., Ilia S., Bovin N., Nicaise M., Desmadril M. // Biochem. J. 2005, V.389, Pt2, P.325-332
  33. Kirkeby S., Hansen A.K., d´Apice A., Moe D. // Microb. Pathog. 2006, V.40, №5, P.191-197
  34. Kirkeby S., Wimmerová M., Moe D., Hansen A.K. // Microbes Infect. 2007, V.9, №5, P.566-573
  35. Imberty A., Wimmerová M., Mitchell E.P., Gilboa-Garber N. // Microbes Infect. 2004, V.6, №2, P.221-228
  36. Wentworth J.S., Austin F.E., Garber N., Gilboa-Garber N., Paterson C.A., Doyle R.J. // Biofouling. 1991, V.4, №1-3, P.99-104
  37. Rebiere-Huët J., Di Martino P., Hulen C. // Can. J. Microbiol. 2004, V.50, №5, P.303-312
  38. Sonawane A., Jyot J., Ramphal R. // Infect. Immun. 2006, V.74, №12, P.7035-7039
  39. Chemani C., Imberty A., de Bentzmann S., Pierre M., Wimmerová M., Guery B.P., Faure K. // Infect. Immun. 2009, V.77, №5, P.2065-2075
  40. Boukerb A.M., Rousset A., Galanos N., Méar J.B., Thépaut M., Grandjean T., Gillon E., Cecioni S., Abderrahmen C., Faure K. // J. Med. Chem. 2014, V.57, №24, P.10275-10289
  41. Nosková L., Kubíčková B., Vašková L., Bláhová B., Wimmerová M., Stiborová M., Hodek P. // Sensors. 2015, V.15, №1, P.1945-1953
  42. Eierhoff T., Bastian B., Thuenauer R., Madl J., Audfray A., Aigal S., Juillot S., Rydell G.E., Müller S., de Bentzmann S. // Proc. Natl. Acad. Sci. USA. 2014, V.111, №35, P.12895-12900
  43. Scharfman A., Arora S.K., Delmotte P., van Brussel E., Mazurier J., Ramphal R., Roussel P. // Infect. Immun. 2001, V.69, №9, P.5243-5248
  44. Hahn H.P. // Gene. 1997, V.192, №1, P.99-108
  45. Diggle S.P., Stacey R.E., Dodd C., Cámara M., Williams P., Winzer K. // Environ. Microbiol. 2006, V.8, №6, P.1095-1104
  46. Johansson E.M.V., Crusz S.A., Kolomiets E., Buts L., Kadam R.U., Cacciarini M., Bartels K.M., Diggle S.P., Cámara M., Williams P. // Chem. Biol. 2008, V.15, №12, P.1249-1257
  47. Ma L., Lu H., Sprinkle A., Parsek M.R., Wozniak D.J. // Journal of Bacteriology 2007, V.189, №22, P.8353-8356
  48. Byrd M.S., Sadovskaya I., Vinogradov E., Lu H., Sprinkle A.B., Richardson S.H., Ma L., Ralston B., Parsek M.R., Anderson E.M. // Mol. Microbiol. 2009, V.73, №4, P.622-638
  49. Ma L., Conover M., Lu H., Parsek M.R., Bayles K., Wozniak D.J. // PLoS Pathog. 2009, V.5, №3, P.e1000354
  50. Bajolet-Laudinat O., Girod-De Bentzmann S.G., Tournier J.M., Madoulet C., Plotkowski M.C., Chippaux C., Puchelle E. // Infect. Immun. 1994, V.62, №10, P.4481-4487
  51. Mewe M., Tielker D., Schönberg R., Schachner M., Jaeger K.E., Schumacher U. // J. Laryngol. Otol. 2005, V.119, №8, P.595-599
  52. Gustke H., Kleene R., Loers G., Nehmann N., Jaehne M., Bartels K.M., Jaeger K.E., Schachner M., Schumacher U. // Eur. J. Clin. Microbiol. Infect. Dis. 2012, V.31, №2, P.207-215
  53. Adam E.C., Mitchell B.S., Schumacher D.U., Grant G., Schumacher U. // Am. J. Respir. Crit. Care Med. 1997, V.155, №6, P.2102-2104
  54. Adam E.C., Schumacher D.U., Schumacher U. // J. Laryngol. Otol. 1997, V.111, №8, P.760-762
  55. Laughlin R.S., Musch M.W., Hollbrook C.J., Rocha F.M., Chang E.B., Alverdy J.C. // Ann. Surg. 2000, V.232, №1, P.133-142
  56. Wu L., Holbrook C., Zaborina O., Ploplys E., Rocha F., Pelham D., Chang E., Musch M., Alverdy J. // Ann. Surg. 2003, V.238, №5, P.754-764
  57. Zinger-Yosovich K.D., Gilboa-Garber N. // J. Agric. Food Chem. 2009, V.57, №15, P.6908-6913
  58. Nurisso A., Blanchard B., Audfray A., Rydner L., Oscarson S., Varrot A., Imberty A. // J. Biol. Chem. 2010, V.285, №26, P.20316-20327
  59. Kadam R.U., Bergmann M., Hurley M., Garg D., Cacciarini M., Swiderska M.A., Nativi C., Sattler M., Smyth A.R., Williams P. // Angew. Chem. Int. Ed. Engl. 2011, V.50, №45, P.10631-10635
  60. Garber N., Guempel U., Belz A., Gilboa-Garber N., Doyle R.J. // Biochim. Biophys. Acta. 1992, V.1116, №3, P.331-333
  61. Stoitsova S.R., Boteva R.N., Doyle R. // Biochim. Biophys. Acta - Gen. Subj. 2003, V.1619, №2, P.213-219
  62. Boteva R.N., Bogoeva V.P., Stoitsova S.R. // Biochim. Biophys. Acta. 2005, V.1747, №2, P.143-149
  63. Loris R., Tielker D., Jaeger K.E., Wyns L. // J. Mol. Biol. 2003, V.331, №4, P.861-870
  64. Garber N., Guempel U., Gilboa-Garber N., Doyle R. // FEMS Microbiol. Lett. 1987, V.48, №3, P.331-334
  65. Sabin C., Mitchell E.P., Pokorná M., Gautier C., Utille J.P., Wimmerová M., Imberty A. // FEBS Lett. 2006, V.580, №3, P.982-987
  66. Lesman-Movshovich E., Lerrer B., Gilboa-Garber N. // Can. J. Microbiol. 2003, V.49, №3, P.230-235
  67. Wu A.M., Wu J.H., Singh T., Liu J.H., Tsai M.S., Gilboa-Garber N. // Biochimie. 2006, V.88, №10, P.1479-1492
  68. Kadam R.U., Garg D., Schwartz J., Visini R., Sattler M., Stocker A., Darbre T., Reymond J.L. // ACS Chem. Biol. 2013, V.8, №9, P.1925-1930
  69. Rodrigue J., Ganne G., Blanchard B., Saucier C., Giguère D., Shiao T.C., Varrot A., Imberty A., Roy R. // Org. Biomol. Chem. 2013, V.11, №40, P.6906-6918
  70. Cecioni S., Praly J.P., Matthews S.E., Wimmerová M., Imberty A., Vidal S. // Chemistry. 2012, V.18, №20, P.6250-6263
  71. Gening M.L., Titov D.V., Cecioni S., Audfray A., Gerbst A.G., Tsvetkov Y.E., Krylov V.B., Imberty A., Nifantiev N.E., Vidal S. // Chemistry. 2013, V.19, №28, P.9272-9285
  72. Marotte K., Sabin C., Préville C., Moumé-Pymbock M., Wimmerová M., Mitchell E.P., Imberty A., Roy R. // ChemMedChem. 2007, V.2, №9, P.1328-1338
  73. Andreini M., Anderluh M., Audfray A., Bernardi A., Imberty A. // Carbohydr. Res. 2010, V.345, №10, P.1400-1407
  74. Hauck D., Joachim I., Frommeyer B., Varrot A., Philipp B., Möller H.M., Imberty A., Exner T.E., Titz A. // ACS Chem. Biol. 2013, V.8, №8, P.1775-1784
  75. Dam T.K., Brewer C.F. // Chem. Rev. 2002, V.102, №2, P.387-429
  76. Wittmann V., Pieters R.J. // Chem. Soc. Rev. 2013, V.42, №10, P.4492-4503
  77. Dam T.K., Brewer C.F. // Adv. Carbohydr. Chem. Biochem. 2010, V.63, №10, P.139-164
  78. Imberty A., Chabre Y.M., Roy R. // Chemistry. 2008, V.14, №25, P.7490-7499
  79. Smadhi M., de Bentzmann S., Imberty A., Gingras M., Abderrahim R., Goekjian P.G. // Beilstein J. Org. Chem. 2014, V.10, P.1981-1990
  80. Cecioni S., Lalor R., Blanchard B., Praly J.P., Imberty A., Matthews S.E., Vidal S. // Chemistry. 2009, V.15, №47, P.13232-13240
  81. Cecioni S., Faure S., Darbost U., Bonnamour I., Parrot-Lopez H., Roy O., Taillefumier C., Wimmerová M., Praly J.P., Imberty A. // Chemistry. 2011, V.17, №7, P.2146-2159
  82. Soomro Z.H., Cecioni S., Blanchard H., Praly J.P., Imberty A., Vidal S., Matthews S.E. // Org. Biomol. Chem. 2011, V.9, №19, P.6587-6597
  83. Cecioni S., Oerthel V., Iehl J., Holler M., Goyard D., Praly J.P., Imberty A., Nierengarten J.F., Vidal S. // Chemistry. 2011, V.17, №11, P.3252-3261
  84. Otsuka I., Blanchard B., Borsali R., Imberty A., Kakuchi T. // ChemBioChem. 2010, V.11, №17, P.2399-2408
  85. Reynolds M., Marradi M., Imberty A., Penadés S., Pérez S. // Chemistry. 2012, V.18, №14, P.4264-4273
  86. Kadam R.U., Bergmann M., Garg D., Gabrieli G., Stocker A., Darbre T., Reymond J.L. // Chemistry. 2013, V.19, №50, P.17054-17063
  87. Chabre Y.M., Giguère D., Blanchard B., Rodrigue J., Rocheleau S., Neault M., Rauthu S., Papadopoulos A., Arnold A.A., Imberty A. // Chemistry. 2011, V.17, №23, P.6545-6562
  88. Gerland B., Goudot A., Ligeour C., Pourceau G., Meyer A., Vidal S., Gehin T., Vidal O., Souteyrand E., Vasseur J.J. // Bioconjug. Chem. 2014, V.25, P.379-392
  89. Pertici F., Pieters R.J. // Chem. Commun. (Camb.). 2012, V.48, №33, P.4008-4010
  90. Pertici F., de Mol N.J., Kemmink J., Pieters R.J. // Chemistry. 2013, V.19, №50, P.16923-16927
  91. Novoa A., Eierhoff T., Topin J., Varrot A., Barluenga S., Imberty A., Römer W., Winssinger N. // Angew. Chem. Int. Ed. Engl. 2014, V.53, №34, P.8885-8889
  92. Morvan F., Meyer A., Jochum A., Sabin C., Chevolot Y., Imberty A., Praly J.P., Vasseur J.J., Souteyrand E., Vidal S. // Bioconjug. Chem. 2007, V.18, №5, P.1637-1643
  93. Berthet N., Thomas B., Bossu I., Dufour E., Gillon E., Garcia J., Spinelli N., Imberty A., Dumy P., Renaudet O. // Bioconjug. Chem. 2013, V.24, №9, P.1598-1611
  94. Kolomiets E., Swiderska M.A., Kadam R.U., Johansson E.M.V., Jaeger K.E., Darbre T., Reymond J.L. // ChemMedChem. 2009, V.4, №4, P.562-569
  95. Johansson E.M.V., Kadam R.U., Rispoli G., Crusz S. A., Bartels K.M., Diggle S.P., Cámara M., Williams P., Jaeger K.E., Darbre T. // Med. Chem. Commun. 2011, V.2, №5, P.418-420
  96. Marotte K., Préville C., Sabin C., Moumé-Pymbock M., Imberty A., Roy R. // Org. Biomol. Chem. 2007, V.5, №18, P.2953-2961
  97. Lerrer B., Gilboa-Garber N. // FEMS Immunol. Med. Microbiol. 2001, V.32, №1, P.33-36
  98. Lerrer B., Gilboa-Garber N. // Electrophoresis. 2002, V.23, №1, P.8-14
  99. Gilboa-Garber N., Zinger-Yosovich K., Lerrer B. // J. ApiProduct ApiMedical Sci. 2009, V.1, №3, P.82-89
  100. Zinger-Yosovich K.D., Iluz D., Sudakevitz D., Gilboa-Garber N. // J. Dairy Sci. 2010, V.93, №2, P.473-482
  101. Rachmaninov O., Zinger-Yosovich K.D., Gilboa-Garber N. // Nutr. J. 2012, V.11, №1, P.10
  102. Grishin A., Karyagina A.S., Tiganova I.G., Dobrynina O.Y., Bolshakova T.N., Boksha I.S., Alexeyeva N.V., Stepanova T.V., Lunin V.G., Chuchalin A.G. // Int. J. Antimicrob. Agents. 2013, V.42, №5, P.471-472
  103. Steuer M.K., Herbst H., Beuth J., Steuer M., Pulverer G., Matthias R. // Oto-Rhino-Laryngologia Nov. 1993, V.3, №1, P.19-25
  104. von Bismarck P., Schneppenheim R., Schumacher U. // Klin. Pädiatrie. 2001, V.213, №5, P.285-287
  105. Hauber H.P., Schulz M., Pforte A., Mack D., Zabel P., Schumacher U. // Int. J. Med. Sci. 2008, V.5, №6, P.371-376

Views

Abstract - 175

PDF (English) - 62

PDF (Russian) - 54

Cited-By


PlumX

Dimensions

Refbacks

  • There are currently no refbacks.

Copyright (c) 2015 Grishin A.V., Krivozubov M.S., Karyagina A.S., Gintsburg A.L.

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies