The therapeutic potential of the humoral pattern recognition molecule PTX3 in chronic lung infection caused by Pseudomonas aeruginosa

Journal of Immunology

Volumn 186, Issue 9, 2011, Pages 5425-5434

  Moalli, Federica ^a   Paroni, Moira ^b   Rodriguez, Tania Véliz ^a   Riva, Federica ^c   Polentarutti, Nadia ^a   Bottazzi, Barbara ^a   Valentino, Sonia ^a   Mantero, Stefano ^a   Nebuloni, Manuela ^d   Mantovani, Alberto ^a,c   Bragonzi, Alessandra ^b   Garlanda, Cecilia ^a  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; FC RECEPTOR; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PENTRAXIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; COLONY FORMING UNIT; CONTROLLED STUDY; DRUG EFFICACY; HISTOPATHOLOGY; HUMORAL IMMUNITY; LUNG ASPERGILLOSIS; LUNG INFECTION; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SURVIVAL RATE; TREATMENT DURATION; TREATMENT RESPONSE;

ANIMALS; C-REACTIVE PROTEIN; CHRONIC DISEASE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOLOGIC FACTORS; MALE; MICE; MICE, INBRED C57BL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY TRACT INFECTIONS; SERUM AMYLOID P-COMPONENT;

EID: 79955525443     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002035     Document Type: Article

References (60)

1. Painter, R. G., V. G. Valentine, N. A. Lanson, Jr., K. Leidal, Q. Zhang, G. Lombard, C. Thompson, A. Viswanathan, W. M. Nauseef, G. Wang, and G. Wang. 2006. CFTR Expression in human neutrophils and the phagolysosomal chlorination defect in cystic fibrosis. Biochemistry 45: 10260-10269. (Pubitemid 44384801)
2. Di, A., M. E. Brown, L. V. Deriy, C. Li, F. L. Szeto, Y. Chen, P. Huang, J. Tong, A. P. Naren, V. Bindokas, et al. 2006. CFTR regulates phagosome acidification in macrophages and alters bactericidal activity. Nat. Cell Biol. 8: 933-944.
3. Döring, G., and E. Gulbins. 2009. Cystic fibrosis and innate immunity: how chloride channel mutations provoke lung disease. Cell. Microbiol. 11: 208-216.
4. Mall, M., B. R. Grubb, J. R. Harkema, W. K. O'Neal, and R. C. Boucher. 2004. Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat. Med. 10: 487-493.
5. Gibson, R. L., J. L. Burns, and B. W. Ramsey. 2003. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168: 918-951.
6. Chmiel, J. F., and M. W. Konstan. 2007. Inflammation and anti-inflammatory therapies for cystic fibrosis. Clin. Chest Med. 28: 331-346.
7. O'Sullivan, B. P., and S. D. Freedman. 2009. Cystic fibrosis. Lancet 373: 1891-1904.
8. Hartl, D., P. Latzin, P. Hordijk, V. Marcos, C. Rudolph, M.Woischnik, S. Krauss-Etschmann, B. Koller, D. Reinhardt, A. A. Roscher, et al. 2007. Cleavage of CXCR1 on neutrophils disables bacterial killing in cystic fibrosis lung disease. Nat. Med. 13: 1423-1430.
9. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2: 1051-1060.
10. Pier, G. B. 2002. CFTR mutations and host susceptibility to Pseudomonas aeruginosa lung infection. Curr. Opin. Microbiol. 5: 81-86.
11. Ichikawa, J. K., A. Norris, M. G. Bangera, G. K. Geiss, A. B. van 't Wout, R. E. Bumgarner, and S. Lory. 2000. Interaction of pseudomonas aeruginosa with epithelial cells: identification of differentially regulated genes by expression microarray analysis of human cDNAs. Proc. Natl. Acad. Sci. USA 97: 9659-9664.
12. McMorran, B., L. Town, E. Costelloe, J. Palmer, J. Engel, D. Hume, and B. Wainwright. 2003. Effector ExoU from the type III secretion system is an important modulator of gene expression in lung epithelial cells in response to Pseudomonas aeruginosa infection. Infect. Immun. 71: 6035-6044.
13. Smith, E. E., D. G. Buckley, Z. Wu, C. Saenphimmachak, L. R. Hoffman, D. A. D'Argenio, S. I. Miller, B. W. Ramsey, D. P. Speert, S. M. Moskowitz, et al. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 103: 8487-8492.
14. Bragonzi, A., M. Paroni, A. Nonis, N. Cramer, S. Montanari, J. Rejman, C. Di Serio, G. Döring, and B. Tümmler. 2009. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am. J. Respir. Crit. Care Med. 180: 138-145.
15. Høiby, N., H. Krogh Johansen, C. Moser, Z. Song, O. Ciofu, and A. Kharazmi. 2001. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect. 3: 23-35. (Pubitemid 32172037)
16. Ratjen, F., and G. Döring. 2003. Cystic fibrosis. Lancet 361: 681-689. (Pubitemid 36246556)
17. Garlanda, C., B. Bottazzi, A. Bastone, and A. Mantovani. 2005. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 23: 337-366.
18. Jaillon, S., G. Peri, Y. Delneste, I. Frémaux, 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.
19. 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. (Pubitemid 35340122)
20. Diniz, S. N., R. Nomizo, P. S. Cisalpino, M. M. Teixeira, G. D. Brown, A. Mantovani, S. Gordon, L. F. Reis, and A. A. Dias. 2004. PTX3 function as an opsonin for the dectin-1-dependent internalization of zymosan by macrophages. J. Leukoc. Biol. 75: 649-656.
21. Souza, D. G., A. C. Soares, V. Pinho, H. Torloni, L. F. Reis, M. M. Teixeira, and A. A. Dias. 2002. Increased mortality and inflammation in tumor necrosis factorstimulated gene-14 transgenic mice after ischemia and reperfusion injury. [Published erratum appears in 2003 Am. J. Pathol. 162: 359.] Am. J. Pathol. 160: 1755-1765. (Pubitemid 34525655)
22. Bozza, S., F. Bistoni, R. Gaziano, L. Pitzurra, T. Zelante, P. Bonifazi, K. Perruccio, S. Bellocchio, M. Neri, A. M. Iorio, et al. 2006. Pentraxin 3 protects from MCMV infection and reactivation through TLR sensing pathways leading to IRF3 activation. Blood 108: 3387-3396.
23. Reading, P. C., S. Bozza, B. Gilbertson, M. Tate, S. Moretti, E. R. Job, E. C. Crouch, A. G. Brooks, L. E. Brown, B. Bottazzi, et al. 2008. Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J. Immunol. 180: 3391-3398.
24. Soares, A. C., D. G. Souza, V. Pinho, A. T. Vieira, J. R. Nicoli, F. Q. Cunha, A. Mantovani, L. F. Reis, A. A. Dias, and M. M. Teixeira. 2006. Dual function of the long pentraxin PTX3 in resistance against pulmonary infection with Klebsiella pneumoniae in transgenic mice. Microbes Infect. 8: 1321-1329.
25. 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.
26. Deban, L., R. C. Russo, M. Sironi, F. Moalli, M. Scanziani, V. Zambelli, I. Cuccovillo, A. Bastone, M. Gobbi, S. Valentino, et al. 2010. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat. Immunol. 11: 328-334.
27. Bottazzi, B., V. Vouret-Craviari, A. Bastone, L. De Gioia, C. Matteucci, G. Peri, F. Spreafico, M. Pausa, C. D'Ettorre, E. Gianazza, et al. 1997. Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins C-reactive protein and serum amyloid P component. J. Biol. Chem. 272: 32817-32823.
28. Nauta, A. J., B. Bottazzi, A. Mantovani, G. Salvatori, U. Kishore, W. J. Schwaeble, A. R. Gingras, S. Tzima, F. Vivanco, J. Egido, et al. 2003. Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur. J. Immunol. 33: 465-473.
29. Roumenina, L. T., M. M. Ruseva, A. Zlatarova, R. Ghai, M. Kolev, N. Olova, M. Gadjeva, A. Agrawal, B. Bottazzi, A. Mantovani, et al. 2006. Interaction of C1q with IgG1, C-reactive protein and pentraxin 3: mutational studies using recombinant globular head modules of human C1q A, B, and C chains. Biochemistry 45: 4093-4104.
30. Deban, L., H. Jarva, M. J. Lehtinen, B. Bottazzi, A. Bastone, A. Doni, T. S. Jokiranta, A. Mantovani, and S. Meri. 2008. Binding of the long pentraxin PTX3 to factor H: interacting domains and function in the regulation of complement activation. J. Immunol. 181: 8433-8440.
31. Ma, Y. J., A. Doni, T. Hummelshøj, C. Honoré, A. Bastone, A. Mantovani, N. M. Thielens, and P. Garred. 2009. Synergy between ficolin-2 and pentraxin 3 boosts innate immune recognition and complement deposition. J. Biol. Chem. 284: 28263-28275.
32. Jeannin, P., B. Bottazzi, M. Sironi, A. Doni, M. Rusnati, M. Presta, V. Maina, G. Magistrelli, J. F. Haeuw, G. Hoeffel, et al. 2005. Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 22: 551-560. (Pubitemid 40719191)
33. Cotena, A., V. Maina, M. Sironi, B. Bottazzi, P. Jeannin, A. Vecchi, N. Corvaia, M. R. Daha, A. Mantovani, and C. Garlanda. 2007. Complement dependent amplification of the innate response to a cognate microbial ligand by the long pentraxin PTX3. J. Immunol. 179: 6311-6317.
34. Bharadwaj, D., M. P. Stein, M. Volzer, C. Mold, and T. W. Du Clos. 1999. The major receptor for C-reactive protein on leukocytes is fcgamma receptor II. J. Exp. Med. 190: 585-590.
35. 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 FcgammaR by innate pentraxins. Nature 456: 989-992.
36. Moalli, F., A. Doni, L. Deban, T. Zelante, S. Zagarella, B. Bottazzi, L. Romani, A. Mantovani, and C. Garlanda. 2010. Role of complement and Fc{gamma} receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 116: 5170-5180.
37. Chiarini, M., C. Sabelli, P. Melotti, C. Garlanda, G. Savoldi, C. Mazza, R. Padoan, A. Plebani, A. Mantovani, L. D. Notarangelo, et al. 2010. PTX3 genetic variations affect the risk of Pseudomonas aeruginosa airway colonization in cystic fibrosis patients. Genes Immun. 11: 665-670.
38. Olesen, R., C. Wejse, D. R. Velez, C. Bisseye, M. Sodemann, P. Aaby, P. Rabna, A. Worwui, H. Chapman, M. Diatta, et al. 2007. DC-SIGN (CD209), pentraxin 3 and vitamin D receptor gene variants associate with pulmonary tuberculosis risk in West Africans. Genes Immun. 8: 456-467. (Pubitemid 47370843)
39. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, et al. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
40. Bragonzi, A., L. Wiehlmann, J. Klockgether, N. Cramer, D. Worlitzsch, G. Döring, and B. Tümmler. 2006. Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 152: 3261-3269. (Pubitemid 44734330)
41. Rivieccio, V., A. Esposito, P. Bellofiore, P. Palladino, M. Sassano, M. Colombo, and A. Verdoliva. 2007. High-level expression and efficient purification of recombinant human long pentraxin PTX3 in Chinese hamster ovary cells. Protein Expr. Purif. 51: 49-58.
42. Cash, H. A., D. E. Woods, B. McCullough, W. G. Johanson, Jr., and J. A. Bass. 1979. A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am. Rev. Respir. Dis. 119: 453-459.
43. Bragonzi, A., D. Worlitzsch, G. B. Pier, P. Timpert, M. Ulrich, M. Hentzer, J. B. Andersen, M. Givskov, M. Conese, and G. Doring. 2005. Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J. Infect. Dis. 192: 410-419.
44. Bragonzi, A. 2010. Murine models of acute and chronic lung infection with cystic fibrosis pathogens. Int. J. Med. Microbiol. 300: 584-593.
45. Konstan, M. W., K. M. Vargo, and P. B. Davis. 1990. Ibuprofen attenuates the inflammatory response to Pseudomonas aeruginosa in a rat model of chronic pulmonary infection. Implications for antiinflammatory therapy in cystic fibrosis. Am. Rev. Respir. Dis. 141: 186-192.
46. Beaulac, C., S. Clément-Major, J. Hawari, and J. Lagacé. 1996. Eradication of mucoid Pseudomonas aeruginosa with fluid liposome-encapsulated tobramycin in an animal model of chronic pulmonary infection. Antimicrob. Agents Chemother. 40: 665-669.
47. Mueller-Ortiz, S. L., S. M. Drouin, and R. A. Wetsel. 2004. The alternative activation pathway and complement component C3 are critical for a protective immune response against Pseudomonas aeruginosa in a murine model of pneumonia. Infect. Immun. 72: 2899-2906.
48. Younger, J. G., S. Shankar-Sinha, M. Mickiewicz, A. S. Brinkman, G. A. Valencia, J. V. Sarma, E. M. Younkin, T. J. Standiford, F. S. Zetoune, and P. A. Ward. 2003. Murine complement interactions with Pseudomonas aeruginosa and their consequences during pneumonia. Am. J. Respir. Cell Mol. Biol. 29: 432-438.
49. Heale, J. P., A. J. Pollard, R. W. Stokes, D. Simpson, A. Tsang, B. Massing, and D. P. Speert. 2001. Two distinct receptors mediate nonopsonic phagocytosis of different strains of Pseudomonas aeruginosa. J. Infect. Dis. 183: 1214-1220.
50. Carlsson, M., A. G. Sjöholm, L. Eriksson, S. Thiel, J. C. Jensenius, M. Segelmark, and L. Truedsson. 2005. Deficiency of the mannan-binding lectin pathway of complement and poor outcome in cystic fibrosis: bacterial colonization may be decisive for a relationship. Clin. Exp. Immunol. 139: 306-313.
51. Zhang, J., J. Koh, J. Lu, S. Thiel, B. S. Leong, S. Sethi, C. Y. He, B. Ho, and J. L. Ding. 2009. Local inflammation induces complement crosstalk which amplifies the antimicrobial response. PLoS Pathog. 5: e1000282.
52. Höpken, U. E., B. Lu, N. P. Gerard, and C. Gerard. 1996. The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 383: 86-89. (Pubitemid 26296466)
53. Rhein, L. M., M. Perkins, N. P. Gerard, and C. Gerard. 2008. FcgammaRIII is protective against Pseudomonas aeruginosa pneumonia. Am. J. Respir. Cell Mol. Biol. 38: 401-406.
54. Kunert, A., J. Losse, C. Gruszin, M. Hühn, K. Kaendler, S. Mikkat, D. Volke, R. Hoffmann, T. S. Jokiranta, H. Seeberger, et al. 2007. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J. Immunol. 179: 2979-2988.
55. Tirouvanziam, R., I. Khazaal, and B. Péault. 2002. Primary inflammation in human cystic fibrosis small airways. Am. J. Physiol. Lung Cell. Mol. Physiol. 283: L445-L451.
56. Sagel, S. D., and F. J. Accurso. 2002. Monitoring inflammation in CF. Cytokines. Clin. Rev. Allergy Immunol. 23: 41-57.
57. Dubin, P. J., and J. K. Kolls. 2007. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L519-L528.
58. McAllister, F., A. Henry, J. L. Kreindler, P. J. Dubin, L. Ulrich, C. Steele, J. D. Finder, J. M. Pilewski, B. M. Carreno, S. J. Goldman, et al. 2005. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogenealpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 175: 404-412. (Pubitemid 40884344)
59. Han, B., J. J. Haitsma, Y. Zhang, X. Bai, M. Rubacha, S. Keshavjee, H. Zhang, and M. Liu. 2011. Long pentraxin PTX3 deficiency worsens LPS-induced acute lung injury. Intensive Care Med. 37: 334-342.
60. Dias, A. A., A. R. Goodman, J. L. Dos Santos, R. N. Gomes, A. Altmeyer, P. T. Bozza, M. F. Horta, J. Vilcek, and L. F. Reis. 2001. TSG-14 transgenic mice have improved survival to endotoxemia and to CLP-induced sepsis. J. Leukoc. Biol. 69: 928-936.