Sialoglycoproteins adsorbed by pseudomonas aeruginosa facilitate their survival by impeding neutrophil extracellular trap through siglec-9

Journal of Leukocyte Biology

Volumn 91, Issue 4, 2012, Pages 641-655

  Khatua, Biswajit ^a   Bhattacharya, Kaushik ^a   Mandal, Chitra ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

Elastase; Innate immunity; Reactive oxygen species; Sialic acids

Indexed keywords

ACETYLCYSTEINE; DEOXYRIBONUCLEASE; ELASTASE; LECTIN; REACTIVE OXYGEN METABOLITE; SIALOGLYCOPROTEIN; SIGLEC 9; SIVELESTAT; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; BINDING AFFINITY; CELL SURFACE; CELL SURVIVAL; CHIMERA; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME RELEASE; HUMAN; HUMAN CELL; INNATE IMMUNITY; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA;

ACETYLCYSTEINE; ADULT; ANIMALS; ANTIGENS, CD; ANTIGENS, CD43; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; FEMALE; FREE RADICAL SCAVENGERS; GLYCINE; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; LECTINS; MALE; NEUTROPHILS; PHAGOCYTOSIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; REACTIVE OXYGEN SPECIES; SERINE PROTEINASE INHIBITORS; SULFONAMIDES;

PSEUDOMONAS AERUGINOSA; SIA;

EID: 84860861243     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0511260     Document Type: Article

References (54)

1. Springer, T. A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76, 301-314.
2. Hampton, M. B., Kettle, A. J., Winterbourn, C. C. (1998) Inside the neu-trophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92, 3007-3017.
3. Nieminen, J., St-Pierre, C., Sato, S. (2005) Galectin-3 interacts with naive and primed neutrophils, inducing innate immune responses. J. Leukoc. Biol. 78, 1127-1135.
4. Ganz, T. (1999) Oxygen-independent microbicidal mechanisms of phagocytes. Proc. Assoc. Am. Physicians 111, 390-395.
5. Bianchi, M., Hakkim, A., Brinkmann, V., Siler, U., Seger, R. A., Zychlin-sky, A., Reichenbach, J. (2009) Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114, 2619-2622.
6. Rifat, S., Kang, T. J., Mann, D., Zhang, L., Puche, A. C., Stamatos, N. M., Goldblum, S. E., Brossmer, R., Cross, A. S. (2008) Expression of sialyl-transferase activity on intact human neutrophils. J. Leukoc. Biol. 84, 1075-1081.
7. Cross, A. S., Sakarya, S., Rifat, S., Held, T. K., Drysdale, B. E., Grange, P. A., Cassels, F. J., Wang, L. X., Stamatos, N., Farese, A., Casey, D., Powell, J., Bhattacharjee, A. K., Kleinberg, M., Goldblum, S. E. (2003) Recruitment of murine neutrophils in vivo through endogenous sialidase activity. J. Biol. Chem. 278, 4112-4120.
8. Crocker, P. R., Paulson, J. C., Varki, A. (2007) Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266.
9. Ravetch, J. V., Lanier, L. L. (2000) Immune inhibitory receptors. Science 290, 84-89.
10. Crocker, P. R., Varki, A. (2001) Siglecs, Siass and innate immunity. Trends Immunol. 22, 337-342.
11. Cao, H., Crocker, P. R. (2011) Evolution of CD33-related siglecs: regulating host immune functions and escaping pathogen exploitation? Immunology 132, 18-26.
12. Lu, W., Hisatsune, A., Koga, T., Kato, K., Kuwahara, I., Lillehoj, E. P., Chen, W., Cross, A. S., Gendler, S. J., Gewirtz, A. T., Kim, K. C. (2006) Cutting edge: enhanced pulmonary clearance of Pseudomonas aeruginosa by Muc1 knockout mice. J. Immunol. 176, 3890-3894.
13. Khatua, B., Ghoshal, A., Bhattacharya, K., Mandal, C., Saha, B., Crocker, P. R., Mandal, C. (2010) Sias acquired by Pseudomonas aeruginosa are involved in reduced complement deposition and siglec mediated host-cell recognition. FEBS Lett. 584, 555-561.
14. Coleman, H. N., Daines, D. A., Jarisch, J., Smith, A. L. (2003) Chemically defined media for growth of Haemophilus influenzae strains. J. Clin. Micro-biol. 41, 4408-4410.
15. Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265-275.
16. Chatterjee, M., Chava, A. K., Kohla, G., Pal, S., Merling, A., Hinderlich, S., Unger, U., Strasser, P., Gerwig, G. J., Kamerling, J. P., Vlasak, R., Crocker, P. R., Schauer, R., Schwartz-Albiez, R., Mandal, C. (2003) Identification and characterization of adsorbed serum sialoglycans on Leishma-nia donovani promastigotes. Glycobiology 13, 351-361.
17. Zhang, J. Q., Nicoll, G., Jones, C., Crocker, P. R. (2000) Siglec-9, a novel sialic acid binding member of the immunoglobulin superfamily expressed broadly on human blood leukocytes. J. Biol. Chem. 275, 22121-22126.
18. Jones, C., Virji, M., Crocker, P. R. (2003) Recognition of sialylated me-ningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol. Microbiol. 49, 1213-1225.
19. Nicoll, G., Ni, J., Liu, D., Klenerman, P., Munday, J., Dubock, S., Mattei, M. G., Crocker, P. R. (1999) Identification and characterization of a novel siglec, siglec-7, expressed by human natural killer cells and mono-cytes. J. Biol. Chem. 274, 34089-34095.
20. Avril, T., Wagner, E. R., Willison, H. J., Crocker, P. R. (2006) Sias-bind-ing immunoglobulin-like lectin 7 mediates selective recognition of sialy-lated glycans expressed on Campylobacter jejuni lipooligosaccharides. Infect. Immun. 74, 4133-4141.
21. Borregaard, N., Heiple, J. M., Simons, E. R., Clark, R. A. (1983) Subcellular localization of the b-cytochrome component of the human neutrophil mi-crobicidal oxidase: translocation during activation. J. Cell Biol. 97, 52-61.
22. Carlin, A. F., Uchiyama, S., Chang, Y. C., Lewis, A. L., Nizet, V., Varki, A. (2009) Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil siglec-9 and dampen the innate immune response. Blood 113, 3333-3336.
23. Peikert, T., Finkielman, J. D., Hummel, A. M., McKenney, M. E., Grego-rini, G., Trimarchi, M., Specks, U. (2008) Functional characterization of antineutrophil cytoplasmic antibodies in patients with cocaine-induced midline destructive lesions. Arthritis Rheum. 58, 1546-1551.
24. Berends, E. T., Horswill, A. R., Haste, N. M., Monestier, M., Nizet, V., von Köckritz-Blickwede, M. (2010) Nuclease expression by Staphylococcus au-reus facilitates escape from neutrophil extracellular traps. J. Innate Immun. 2, 576-586.
25. Papayannopoulos, V., Metzler, K. D., Hakkim, A., Zychlinsky, A. (2010) Neutrophil elastase and myeloperoxidase regulate the formation of neu-trophil extracellular traps. J. Cell Biol. 191, 677-691.
26. Vasseur, P., Vallet-Gely, I., Soscia, C, Genin, S., Filloux, A. (2005) The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151, 985-997.
27. Sillanaukee, P., Pönniö, M., Jääskeläainen, I. P. (1999) Occurrence of sialic acids in healthy humans and different disorders. Eur. J. Clin. Invest. 29, 413-425.
28. Crook, M. A., Pickup, J. C, Lumb, P. J., Giorgino, F., Webb, D. J., Fuller, J. H. (2001) Relationship between plasma sialic acid concentration and microvascular and macrovascular complications in type 1 diabetes. Diabetes Care 24, 316-322.
29. Severi, E., Hood, D. W., Thomas, G. H. (2007) Sias utilization by bacterial pathogens. Microbiology 153, 2817-2822.
30. Chava, A. K, Chatterjee, M., Gerwig, G. J., Kamerling, J. P., Mandal, C. (2004) Identification of sialic acids on Leishmania donovani amastigotes. Biol. Chem. 385, 59-66.
31. Tiralongo, E., Martensen, I., Grötzinger, J., Tiralongo, J., Schauer, R. (2002) Trans-sialidase-like sequences from Trypanosoma congolense con serve most of the critical active site residues found in other trans-siali- dases. Biol. Chem. 384, 1203-1213.
32. Carlin, A. F., Chang, Y. C, Areschoug, T., Lindahl, G., Hurtado-Ziola, N., King, C. C, Varki, A, Nizet, V. (2009) Group B Streptococcus suppression of phagocyte functions by protein-mediated engagement of human siglec-5. J. Exp. Med. 206, 1691-1699.
33. Graham, D. B., Robertson, C. M., Bautista, J., Mascarenhas, F., Diacovo, M. J., Montgrain, V., Lam, S. K, Cremasco, V., Dunne, W. M., Faccio, R, Coopersmith, C. M., Swat, W. (2007) Neutrophil-mediated oxidative burst and host defense are controlled by a Vav-PLCγ2 signaling axis in mice. J. Clin. Invest. 117, 3445-3452.
34. Belaaouaj, A, Kim, K. S., Shapiro, S. D. (2000) Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase. Science 289, 1185-1188.
35. Niemann, C. U., Abrink, M., Pejler, G., Fischer, R L., Christensen, E. I., Knight, S. D., Borregaard, N. (2007) Neutrophil elastase depends on ser-glycin proteoglycan for localization in granules. Blood 109, 4478-4486.
36. Hirche, T. O., Benabid, R, Deslee, G., Gangloff, S., Achilefu, S., Gue-nounou, M., Lebargy, F., Hancock, R E., Belaaouaj, A. (2008) Neutrophil elastase mediates innate host protection against. Pseudomonas aeruginosa. J. Immunol. 181, 4945-4954.
37. Balloy, V., Sallenave, J. M., Crestani, B., Dehoux, M., Chignard, M. (2003) Neutrophil DNA contributes to the antielastase barrier during acute lung inflammation. Am. J. Respir. Cell Mol. Biol. 28, 746-753.
38. Carlin, A. F., Lewis, A. L., Varki, A, Nizet, V. (2007) Group B streptococcal capsular sialic acids interact with siglecs (immunoglobulin-like lectins) on human leukocytes. J. Bacteriol. 189, 1231-1237.
39. Heikema, A. P., Bergman, M. P., Richards, H., Crocker, P. R, Gilbert, M., Samsom, J. N., van Wamel, W. J., Endtz, H. P., van Belkum, A. (2010) Characterization of the specific interaction between sialoadhesin and sia-lylated Campylobacter jejuni lipooligosaccharides. Infect. Immun. 78, 3237-3246.
40. Goller, C. C, Seed, P. C. (2010) Revisiting the Escherichia coli polysaccharide capsule as a virulence factor during urinary tract infection: contribution to intracellular biofilm development. Virulence 1, 333-337.
41. Johnston, J. W., Coussens, N. P., Allen, S., Houtman, J. C, Turner, K. H., Zaleski, A, Ramaswamy, S., Gibson, B. W., Apicella, M. A. (2008) Characterization of the N-acetyl-5-neuraminic acid-binding site of the extracyto-plasmic solute receptor (SiaP) of nontypeable Haemophilus influenzae strain 2019. J. Biol. Chem. 283, 855-865.
42. Goon, S., Schilling, B., Tullius, M. V., Gibson, B. W., Bertozzi, C. R. (2003) Metabolic incorporation of unnatural sialic acids into Haemophilus ducreyi lipooligosaccharides. Proc. Natl. Acad. Sci. USA 100, 3089-3094.
43. Diallo, I. S., Frost, A. J. (2000) Survival of avian strains of Pasteurella mul-tocida in chicken serum. Vet. Microbiol. 72, 153-161.
44. Buchanan, J. T., Simpson, A. J., Aziz, R. K., Liu, G. Y., Kristian, S. A., Kotb, M., Feramisco, J., Nizet, V. (2006) DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 16, 396-400.
45. Wartha, F., Beiter, K., Albiger, B., Fernebro, J., Zychlinsky, A., Normark, S., Henriques-Normark, B. (2007) Capsule and d-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell. Microbiol. 9, 1162-1171.
46. Simons, M. P., Nauseef, W. M., Apicella, M. A. (2005) Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect. Immun. 73, 1971-1977.
47. Li, P., Li, M., Lindberg, M. R., Kennett, M. J., Xiong, N., Wang, Y. (2010) PAD4 is essential for antibacterial innate immunity mediated by neutro-phil extracellular traps. J. Exp. Med. 207, 1853-1862.
48. Nagl, M., Kacani, L., Müllauer, B., Lemberger, E. M., Stoiber, H., Sprinzl, G. M., Schennach, H., Dierich, M. P. (2002) Phagocytosis and killing of bacteria by professional phagocytes and dendritic cells. Clin. Diagn. Lab. Immunol. 9, 1165-1168.
49. Gibson, R. L., Burns, J. L., Ramsey, B. W. (2003) Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168, 918-951.
50. Sedivá, A., Bartůnková, J., Bartosová, J., Jennette, C., Falk, R. J., Jethwa, H. S. (2003) Antineutrophil cytoplasmic antibodies directed against bactericidal/permeability-increasing protein detected in children with cystic fibrosis inhibit neutrophil-mediated killing of Pseudomonas aeruginosa. Microbes Infect. 5, 27-30.
51. Usher, L. R., Lawson, R. A., Geary, I., Taylor, C. J., Bingle, C. D., Taylor, G. W., Whyte, M. K. B. (2002) Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: a potential mechanism of persistent infection. J. Immunol. 168, 1861-1868.
52. Greiner, L. L., Watanabe, H., Phillips, N. J., Shao, J., Morgan, A., Zaleski, A., Gibson, B. W., Apicella, M. A. (2004) Nontypeable Haemophilus influ-enzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans. Infect. Immun. 72, 4249-4260.
53. De Santo, C., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R., Salio, M., Middleton, M., Cerundolo, V. (2010) Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 11, 1039-1046.
54. Ando, M., Tu, W., Nishijima, K., Iijima, S. (2008) Siglec-9 enhances IL-10 production in macrophages via tyrosine-based motifs. Biochem. Biophys. Res. Commun. 369, 878-883.