Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease

Journal of Immunology

Volumn 183, Issue 7, 2009, Pages 4609-4618

  D'Angelo, Carmen ^a   De Luca, Antonella ^a   Zelante, Teresa ^a   Bonifazi, Pierluigi ^a   Moretti, Silvia ^a   Giovannini, Gloria ^a   Iannitti, Rossana Giulietta ^a   Zagarella, Silvia ^a   Bozza, Silvia ^a   Campo, Silvia ^b   Salvatori, Giovanni ^b   Romani, Luigina ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b Sigma Tau SpA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 23 RECEPTOR; PENTRAXIN 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TUMOR NECROSIS FACTOR ALPHA; VORICONAZOLE; ANTIFUNGAL AGENT; AUTACOID; C REACTIVE PROTEIN; SERUM AMYLOID P;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ARTICLE; ASPERGILLOSIS; CELL EXPANSION; CELLULAR IMMUNITY; CHRONIC GRANULOMATOUS DISEASE; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; DRUG POTENCY; EPITHELIUM CELL; IMMUNOPATHOLOGY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 CELL; TH17 CELL; ANIMAL; ASPERGILLUS FUMIGATUS; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CHO CELL; CRICETULUS; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; IMMUNOLOGY; LUNG ASPERGILLOSIS; METABOLISM; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY;

ANIMALS; ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; C-REACTIVE PROTEIN; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; DRUG RESISTANCE, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; GRANULOMATOUS DISEASE, CHRONIC; INFLAMMATION MEDIATORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PULMONARY ASPERGILLOSIS; SERUM AMYLOID P-COMPONENT;

EID: 70449723403     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900345     Document Type: Article

References (60)

1. Segal, B. H., T. L. Leto, J. I. Gallin, H. L. Malech, and S. M. Holland. 2000. Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine 79: 170-200.
2. Siddiqui, S., V. L. Anderson, D. M. Hilligoss, M. Abinun, T. W. Kuijpers, H. Masur, F. G. Witebsky, Y. R. Shea, J. I. Gallin, H. L. Malech, and S. M. Holland. 2007. Fulminant mulch pneumonitis: an emergency presentation of chronic granulomatous disease. Clin. Infect. Dis. 45: 673-681.
3. Gallin, J. I., and K. Zarember. 2007. Lessons about the pathogenesis and management of aspergillosis from studies in chronic granulomatous disease. Trans. Am. Clin. Climatol. Assoc. 118: 175-185.
4. Schappi, M. G., V. Jaquet, D. C. Belli, and K. H. Krause. 2008. Hyperinflammation in chronic granulomatous disease and anti-inflammatory role of the phagocyte NADPH oxidase. Semin. Immunopathol. 30: 255-271.
5. Almyroudis, N. G., S. M. Holland, and B. H. Segal. 2005 Invasive aspergillosis in primary immunodeficiencies. Med. Mycol. 43 Suppl. 1: S247-S259.
6. George-Chandy, A., I. Nordstrom, E. Nygren, I. M. Jonsson, J. Postigo, L. V. Collins, and K. Eriksson. 2008. Th17 development and autoimmune arthritis in the absence of reactive oxygen species. Eur. J. Immunol. 38: 1118-1126.
7. Griffiths, H. R. 2008. Is the generation of neo-antigenic determinants by free radicals central to the development of autoimmune rheumatoid disease? Autoimmun. Rev. 7: 544-549.
8. phox-/- mice. Infect. Immun. 73: 5204-5207.
9. Romani, L., F. Fallarino, A. De Luca, C. Montagnoli, C. D'Angelo, T. Zelante, C. Vacca, F. Bistoni, M. C. Fioretti, U. Grohmann, et al. 2008. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451: 211-215.
10. Grohmann, U., F. Fallarino, and P. Puccetti. 2003. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol. 24: 242-248.
11. Mellor, A. L., and D. H. Munn. 2004. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4: 762-774.
12. Montagnoli, C., F. Fallarino, R. Gaziano, S. Bozza, S. Bellocchio, T. Zelante, W. P. Kurup, L. Pitzurra, P. Puccetti, and L. Romani. 2006. Immunity and tolerance to Aspergillus involve functionally distinct regulatory T cells and tryptophan catabolism. J. Immunol. 176: 1712-1723. (Pubitemid 43134316)
13. Stone, T. W., and L. G. Darlington. 2002. Endogenous kynurenines as targets for drug discovery and development. Nat. Rev. Drug Discov. 1: 609-620. (Pubitemid 37361524)
14. Zelante, T., A. De Luca, P. Bonifazi, C. Montagnoli, S. Bozza, S. Moretti, M. L. Belladonna, C. Vacca, C. Conte, P. Mosci, et al. 2007. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur. J. Immunol. 37: 2695-2706.
15. Romani, L., T. Zelante, A. De Luca, F. Fallarino, and P. Puccetti. 2008. IL-17 and therapeutic kynurenines in pathogenic inflammation to fungi. J. Immunol. 180: 5157-5162.
16. Seger, R. A. 2008. Modern management of chronic granulomatous disease. Br. J. Haematol. 140: 255-266.
17. Ott, M. G., M. Schmidt, K. Schwarzwaelder, S. Stein, U. Siler, U. Koehl, H. Glimm, K. Kuhlcke, A. Schilz, H. Kunkel, et al. 2006. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat. Med. 12: 401-409.
18. Ott, M. G., R. Seger, S. Stein, U. Siler, D. Hoelzer, and M. Grez. 2007. Advances in the treatment of chronic granulomatous disease by gene therapy. Curr. Gene Ther. 7: 155-161. (Pubitemid 46902198)
19. Segal, B. H., J. Kwon-Chung, T. J. Walsh, B. S. Klein, M. Battiwalla, N. G. Almyroudis, S. M. Holland, and L. Romani. 2006. Immunotherapy for fungal infections. Clin. Infect. Dis. 42: 507-515.
20. Garlanda, C., E. Hirsch, S. Bozza, A. Salustri, M. De Acetis, R. Nota, A. Maccagno, F. Riva, B. Bottazzi, G. Peri, et al. 2002. Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420: 182-186.
21. Manfredi, A. A., P. Rovere-Querini, B. Bottazzi, C. Garlanda, and A. Mantovani. 2008. Pentraxins, humoral innate immunity and tissue injury. Curr. Opin. Immunol. 20: 538-544.
22. Lu, J., L. L. Marnell, K. D. Marjon, C. Mold, T. W. Du Clos, and P. D. Sun. 2008. Structural recognition and functional activation of FcγR by innate pentraxins. Nature 456: 989-992.
23. phox-/- mice: implications for fungal pathogenicity and host defense in chronic granulomatous disease. J. Clin. Invest. 101: 1843-1850.
24. phox-/- mouse model of chronic granulomatous disease. Antimicrob. Agents Chemother. 50: 422-427.
25. Pollock, J. D., D. A. Williams, M. A. Gifford, L. L. Li, X. Du, J. Fisherman, S. H. Orkin, C. M. Doerschuk, and M. C. Dinauer. 1995. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat. Genet. 9: 202-209.
26. Gaziano, R., S. Bozza, S. Bellocchio, K. Perruccio, C. Montagnoli, L. Pitzurra, G. Salvatori, R. De Santis, P. Carminati, A. Mantovani, and L. Romani. 2004. Anti-Aspergillus fumigatus efficacy of pentraxin 3 alone and in combination with antifungals. Antimicrob. Agents Chemother. 48: 4414-4421.
27. Bellocchio, S., S. Moretti, K. Perruccio, F. Fallarino, S. Bozza, C. Montagnoli, P. Mosci, G. B. Lipford, L. Pitzurra, and L. Romani. 2004. TLRs govern neutrophil activity in aspergillosis. J. Immunol. 173: 7406-7415. (Pubitemid 39628180)
28. You, Y., E. J. Richer, T. Huang, and S. L. Brody. 2002. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. 283: L1315-L1321.
29. Bozza, S., T. Zelante, S. Moretti, P. Bonifazi, A. Deluca, C. D'Angelo, G. Giovannini, C. Garlanda, L. Boon, F. Bistoni, et al. 2008. Lack of Toll IL-1R8 exacerbates Th17 cell responses in fungal infection. J. Immunol. 180: 4022-4031.
30. Jaillon, S., G. Peri, Y. Delneste, I. Fremaux, A. Doni, F. Moalli, C. Garlanda, L. Romani, H. Gascan, S. Bellocchio, et al. 2007. The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J. Exp. Med. 204: 793-804.
31. Mauri, T., A. Coppadoro, G. Bellani, M. Bombino, N. Patroniti, G. Peri, A. Mantovani, and A. Pesenti. 2008. Pentraxin 3 in acute respiratory distress syndrome: an early marker of severity. Crit. Care Med. 36: 2302-2308.
32. Souza, D. G., F. A. Amaral, C. T. Fagundes, F. M. Coelho, R. M. Arantes, L. P. Sousa, M. M. Matzuk, C. Garlanda, A. Mantovani, A. A. Dias, and M. M. Teixeira. 2009. The long pentraxin PTX3 is crucial for tissue inflammation after intestinal ischemia and reperfusion in mice. Am. J. Pathol. 174: 1309-1318.
33. Herr, C., R. Shaykhiev, and R. Bals. 2007. The role of cathelicidin and defensins in pulmonary inflammatory diseases. Expert. Opin. Biol. Ther. 7: 1449-1461. (Pubitemid 47485151)
34. Hiemstra, P. S. 2007. The role of epithelial β-defensins and cathelicidins in host defense of the lung. Exp. Lung Res. 33: 537-542. (Pubitemid 350256088)
35. Kato, A., and R. P. Schleimer. 2007. Beyond inflammation: airway epithelial cells are at the interface of innate and adaptive immunity. Curr. Opin. Immunol. 19: 711-720. (Pubitemid 350236807)
36. Linden, A., M. Laan, and G. P. Anderson. 2005. Neutrophils, interleukin-17A and lung disease. Eur. Respir. J. 25: 159-172.
37. Umemura, M., A. Yahagi, S. Hamada, M. D. Begum, H. Watanabe, K. Kawakami, T. Suda, K. Sudo, S. Nakae, Y. Iwakura, and G. Matsuzaki. 2007. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178: 3786-3796.
38. Gallin, J. I., D. W. Alling, H. L. Malech, R. Wesley, D. Koziol, B. Marciano, E. M. Eisenstein, M. L. Turner, E. S. DeCarlo, J. M. Starling, and S. M. Holland. 2003. Itraconazole to prevent fungal infections in chronic granulomatous disease. N. Engl. J. Med. 348: 2416-2422.
39. Born, W. K., C. L. Reardon, and R. L. O'Brien. 2006. The function of γδ T cells in innate immunity. Curr. Opin. Immunol. 18: 31-38.
40. Komori, H. K., T. F. Meehan, and W. L. Havran. 2006. Epithelial and mucosal γδ T cells. Curr. Opin. Immunol. 18: 534-538.
41. Romani, L. 2004 Immunity to fungal infections. Nat. Rev. Immunol. 4 1-23.
42. Ziegler, H. K. 2004. The role of γ/δ T cells in immunity to infection and regulation of inflammation. Immunol. Res. 29: 293-302.
43. Roark, C. L., P. L. Simonian, A. P. Fontenot, W. K. Born, and R. L. O'Brien. 2008. γδ T cells: an important source of IL-17. Curr. Opin. Immunol. 20: 353-357.
44. McGeachy, M. J., and D. J. Cua. 2007. The link between IL-23 and Th17 cell-mediated immune pathologies. Semin. Immunol. 19: 372-376.
45. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8: 950-957.
46. Khader, S. A., J. E. Pearl, K. Sakamoto, L. Gilmartin, G. K. Bell, D. M. Jelley-Gibbs, N. Ghilardi, F. deSauvage, and A. M. Cooper. 2005. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-γ responses if IL-12p70 is available. J. Immunol. 175: 788-795.
47. Holt, P. G., D. H. Strickland, M. E. Wikstrom, and F. L. Jahnsen. 2008. Regulation of immunological homeostasis in the respiratory tract. Nat. Rev. Immunol. 8: 142-152.
48. Schutte, B. C., and P. B. McCray, Jr. 2002. β-defensins in lung host defense. Annu. Rev. Physiol. 64: 709-748.
49. Yang, D., O. Chertov, S. N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schroder, J. M. Wang, O. M. Howard, and J. J. Oppenheim. 1999. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286: 525-528.
50. Bals, R., X. Wang, Z. Wu, T. Freeman, V. Bafna, M. Zasloff, and J. M. Wilson. 1998. Human β-defensin 2 is a salt-sensitive peptide antibiotic expressed in human lung. J. Clin. Invest. 102: 874-880. (Pubitemid 28419232)
51. Singh, P. K., B. F. Tack, P. B. McCray, Jr., and M. J. Welsh. 2000. Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am. J. Physiol. 279: L799-L805.
52. Tkalcevic, J., M. Novelli, M. Phylactides, J. P. Iredale, A. W. Segal, and J. Roes. 2000. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 12: 201-210. (Pubitemid 30398634)
53. Zarember, K. A., J. A. Sugui, Y. C. Chang, K. J. Kwon-Chung, and J. I. Gallin. 2007. Human polymorphonuclear leukocytes inhibit Aspergillus fumigatus conidial growth by lactoferrin-mediated iron depletion. J. Immunol. 178: 6367-6373.
54. Donini, M., E. Zenaro, N. Tamassia, and S. Dusi. 2007. NADPH oxidase of human dendritic cells: role in Candida albicans killing and regulation by interferons, dectin-1 and CD206. Eur. J. Immunol. 37: 1194-1203.
55. Vulcano, M., S. Dusi, D. Lissandrini, R. Badolato, P. Mazzi, E. Riboldi, E. Borroni, A. Calleri, M. Donini, A. Plebani, et al. 2004. Toll receptor-mediated regulation of NADPH oxidase in human dendritic cells. J. Immunol. 173: 5749-5756.
56. Watts, C. 2006. Phagosome neutrality in host defense. Cell 126: 17-19.
57. Gerosa, F., B. Baldani-Guerra, L. A. Lyakh, G. Batoni, S. Esin, R. T. Winkler-Pickett, M. R. Consolaro, M. De Marchi, D. Giachino, A. Robbiano, et al. 2008. Differential regulation of interleukin 12 and interleukin 23 production in human dendritic cells. J. Exp. Med. 205: 1447-1461.
58. Pulendran, B., H. Tang, and T. L. Denning. 2008. Division of labor, plasticity, and crosstalk between dendritic cell subsets. Curr. Opin. Immunol. 20: 61-67.
59. Stark, M. A., Y. Huo, T. L. Burcin, M. A. Morris, T. S. Olson, and K. Ley. 2005. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22: 285-294.
60. Rovere, P., G. Peri, F. Fazzini, B. Bottazzi, A. Doni, A. Bondanza, V. S. Zimmermann, C. Garlanda, U. Fascio, M. G. Sabbadini, et al. 2000. The long pentraxin PTX3 binds to apoptotic cells and regulates their clearance by antigen-presenting dendritic cells. Blood 96: 4300-4306.