Adaptive immune defects against glycoantigens in chronic granulomatous disease via dysregulated nitric oxide production

European Journal of Immunology

Volumn 41, Issue 9, 2011, Pages 2562-2572

  Lewis, Colleen J ^a   Cobb, Brian A ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen presentation processing; Immunodeficiencies; Inflammation

Indexed keywords

BETA ACTIN; CARBOHYDRATE ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ABSCESS; ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CHRONIC GRANULOMATOUS DISEASE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DISEASE SEVERITY; IMMUNE DEFICIENCY; IN VITRO STUDY; IN VIVO STUDY; INCIDENCE; INFECTION SENSITIVITY; INFLAMMATION; MOUSE; MUTATION; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECURRENT DISEASE; T LYMPHOCYTE; TH1 CELL;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; AMIDINES; ANIMALS; ANTIGEN PRESENTATION; BENZYLAMINES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GLYCOPROTEINS; GRANULOMA; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; INTERFERON-GAMMA; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TH1 CELLS;

EID: 80052176419     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141396     Document Type: Article

References (47)

1. Stuehr, D. J., Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1999. 1411: 217-230.
2. Bogdan, C., Nitric oxide and the immune response. Nat. Immunol. 2001. 2: 907-916.
3. Segal, A. W., The function of the NADPH oxidase of phagocytes and its relationship to other NOXs in plants, invertebrates, and mammals. Int. J. Biochem. Cell Biol. 2008. 40: 604-618.
4. Shatwell, K. P. and Segal, A. W., NADPH oxidase. Int. J. Biochem. Cell Biol. 1996. 28: 1191-1195.
5. Ellson, C. D., Davidson, K., Ferguson, G. J., O'Connor, R., Stephens, L. R., and Hawkins, P. T., Neutrophils from p40phox-/- mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing. J. Exp. Med. 2006. 203: 1927-1937.
6. Matute, J. D., Arias, A. A., Wright, N. A., Wrobel, I., Waterhouse, C. C., Li, X. J., Marchal, C. C. et al., A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity. Blood 2009. 114: 3309-3315.
7. Segal, B. H., Leto, T. L., Gallin, J. I., Malech, H. L., and Holland, S. M., Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine (Baltimore) 2000. 79: 170-200.
8. Seger, R. A., Modern management of chronic granulomatous disease. Br. J. Haematol. 2008. 140: 255-266.
9. Rosenzweig, S. D., Inflammatory manifestations in chronic granulomatous disease (CGD). J. Clin. Immunol. 2008. 28: S67-S72.
10. Dinauer, M. C., Chronic granulomatous disease and other disorders of phagocyte function. Hematology (Am. Soc. Hematol. Educ. Program.) 2005. 89-95.
11. Schappi, M. G., Jaquet, V., Belli, D. C., and Krause, K. H., Hyperinflammation in chronic granulomatous disease and anti-inflammatory role of the phagocyte NADPH oxidase. Semin. Immunopathol. 2008. 30: 255-271.
12. Tzianabos, A. O. and Kasper, D. L., Role of T cells in abscess formation. Curr. Opin. Microbiol. 2002. 5: 92-96.
13. Huang, A., Abbasakoor, F., and Vaizey, C. J., Gastrointestinal manifestations of chronic granulomatous disease. Colorectal Dis. 2006. 8: 637-644.
14. Polk, B. F. and Kasper, D. L., Bacteroides fragilis subspecies in clinical isolates. Ann. Intern. Med. 1977. 86: 569-571.
15. Tzianabos, A. O., Onderdonk, A. B., Rosner, B., Cisneros, R. L., and Kasper, D. L., Structural features of polysaccharides that induce intra-abdominal abscesses. Science 1993. 262: 416-419.
16. Tzianabos, A. O., Wang, J. Y., and Lee, J. C., Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides. Proc. Natl. Acad. Sci. USA 2001. 98: 9365-9370.
17. Baumann, H., Tzianabos, A. O., Brisson, J. R., Kasper, D. L., and Jennings, H. J., Structural elucidation of two capsular polysaccharides from one strain of Bacteroides fragilis using high-resolution NMR spectroscopy. Biochemistry 1992. 31: 4081-4089.
18. Kreisman, L. S., Friedman, J. H., Neaga, A., and Cobb, B. A., Structure and function relations with a T-cell-activating polysaccharide antigen using circular dichroism. Glycobiology 2007. 17: 46-55.
19. Wang, Q., McLoughlin, R. M., Cobb, B. A., Charrel-Dennis, M., Zaleski, K. J., Golenbock, D., Tzianabos, A. O. et al., A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 2006. 203: 2853-2863.
20. Cobb, B. A., Wang, Q., Tzianabos, A. O., and Kasper, D. L., Polysaccharide processing and presentation by the MHCII pathway. Cell 2004. 117: 677-687.
21. Duan, J., Avci, F. Y., and Kasper, D. L., Microbial carbohydrate depolymerization by antigen-presenting cells: deamination prior to presentation by the MHCII pathway. Proc. Natl. Acad. Sci. USA 2008. 105: 5183-5188.
22. Cobb, B. A. and Kasper, D. L., Characteristics of carbohydrate antigen binding to the presentation protein HLA-DR. Glycobiology 2008. 18: 707-718.
23. Velez, C. D., Lewis, C. J., Kasper, D. L., and Cobb, B. A., Type I Streptococcus pneumoniae carbohydrate utilizes a nitric oxide and MHC II-dependent pathway for antigen presentation. Immunology 2009. 127: 73-82.
24. Chung, D. R., Kasper, D. L., Panzo, R. J., Chitnis, T., Grusby, M. J., Sayegh, M. H., and Tzianabos, A. O., CD4+T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism. J. Immunol. 2003. 170: 1958-1963.
25. Kalka-Moll, W. M., Tzianabos, A. O., Wang, Y., Carey, V. J., Finberg, R. W., Onderdonk, A. B., and Kasper, D. L., Effect of molecular size on the ability of zwitterionic polysaccharides to stimulate cellular immunity. J. Immunol. 2000. 164: 719-724.
26. Tzianabos, A. O., Russell, P. R., Onderdonk, A. B., Gibson, F. C., III, Cywes, C., Chan, M., Finberg, R. W. et al., IL-2 mediates protection against abscess formation in an experimental model of sepsis. J. Immunol. 1999. 163: 893-897.
27. Fernandez-Boyanapalli, R. F., Frasch, S. C., McPhillips, K., Vandivier, R. W., Harry, B. L., Riches, D. W., Henson, P. M. et al., Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine-dependent production of IL-4. Blood 2009. 113: 2047-2055.
28. Hampton, M. B., Vissers, M. C., Keenan, J. I., and Winterbourn, C. C., Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J. Leukoc. Biol. 2002. 71: 775-781.
29. Arroyo, A., Modriansky, M., Serinkan, F. B., Bello, R. I., Matsura, T., Jiang, J., Tyurin, V. A. et al., NADPH oxidase-dependent oxidation and externalization of phosphatidylserine during apoptosis in Me2SO-differentiated HL-60 cells. Role in phagocytic clearance. J. Biol. Chem. 2002. 277: 49965-49975.
30. Kasper, D. L. and Onderdonk, A. B., Infection with Bacteroides fragilis: pathogenesis and immunoprophylaxis in an animal model. Scand. J. Infect. Dis. Suppl. 1982. 31: 28-33.
31. Bartlett, J. G., Onderdonk, A. B., Louie, T., Kasper, D. L., and Gorbach, S. L., A review. Lessons from an animal model of intra-abdominal sepsis. Arch. Surg. 1978. 113: 853-857.
32. Kielian, T., Haney, A., Mayes, P. M., Garg, S., and Esen, N., Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect. Immun. 2005. 73: 7428-7435.
33. Sanford, A. N., Suriano, A. R., Herche, D., Dietzmann, K., and Sullivan, K. E., Abnormal apoptosis in chronic granulomatous disease and autoantibody production characteristic of lupus. Rheumatology (Oxford) 2006. 45: 178-181.
34. Brown, J. R., Goldblatt, D., Buddle, J., Morton, L., and Thrasher, A. J., Diminished production of anti-inflammatory mediators during neutrophil apoptosis and macrophage phagocytosis in chronic granulomatous disease (CGD). J. Leukoc. Biol. 2003. 73: 591-599.
35. Savina, A., Jancic, C., Hugues, S., Guermonprez, P., Vargas, P., Moura, I. C., Lennon-Dumenil, A. M. et al., NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006. 126: 205-218.
36. Lekstrom-Himes, J. A., Kuhns, D. B., Alvord, W. G., and Gallin, J. I., Inhibition of human neutrophil IL-8 production by hydrogen peroxide and dysregulation in chronic granulomatous disease. J. Immunol. 2005. 174: 411-417.
37. Tsuji, S., Taniuchi, S., Hasui, M., Yamamoto, A., and Kobayashi, Y., Increased nitric oxide production by neutrophils from patients with chronic granulomatous disease on trimethoprim-sulfamethoxazole. Nitric Oxide. 2002. 7: 283-288.
38. Bylund, J., MacDonald, K. L., Brown, K. L., Mydel, P., Collins, L. V., Hancock, R. E., and Speert, D. P., Enhanced inflammatory responses of chronic granulomatous disease leukocytes involve ROS-independent activation of NF-kappa B. Eur. J. Immunol. 2007. 37: 1087-1096.
39. Cobb, B. A. and Kasper, D. L., Zwitterionic capsular polysaccharides: the new MHCII-dependent antigens. Cell Microbiol. 2005. 7: 1398-1403.
40. Lewis, C. J. and Cobb, B. A., Carbohydrate oxidation acidifies endosomes, regulating antigen processing and TLR9 signaling. J. Immunol. 2010. 184: 3789-3800.
41. Meissner, F., Seger, R. A., Moshous, D., Fischer, A., Reichenbach, J., and Zychlinsky, A., Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 2010. 116: 1570-1573.
42. Segal, B. H., Han, W., Bushey, J. J., Joo, M., Bhatti, Z., Feminella, J., Dennis, C. G. et al., NADPH oxidase limits innate immune responses in the lungs in mice. PLoS One 2010. 5: e9631.
43. Efimova, O., Szankasi, P., and Kelley, T. W., Ncf1 (p47phox) is essential for direct regulatory T cell mediated suppression of CD4+effector T cells. PLoS One 2011. 6: e16013.
44. Kraaij, M. D., Savage, N. D., van der Kooij, S. W., Koekkoek, K., Wang, J., van den Berg, J. M., Ottenhoff, T. H. et al., Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc. Natl. Acad. Sci. USA 2010. 107: 17686-17691.
45. van der Veen, R. C., Dietlin, T. A., Hofman, F. M., Pen, L., Segal, B. H., and Holland, S. M., Superoxide prevents nitric oxide-mediated suppression of helper T lymphocytes: decreased autoimmune encephalomyelitis in nicotinamide adenine dinucleotide phosphate oxidase knockout mice. J. Immunol. 2000. 164: 5177-5183.
46. Tzianabos, A. O., Pantosti, A., Baumann, H., Brisson, J. R., Jennings, H. J., and Kasper, D. L., The capsular polysaccharide of Bacteroides fragilis comprises two ionically linked polysaccharides. J. Biol. Chem. 1992. 267: 18230-18235.
47. Harlow, E. and Lane, D., Immunoblotting. Using Antibodies, A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 1999, pp. 269-309.