NADPH oxidase derived reactive oxygen species are involved in human neutrophil IL-1β secretion but not in inflammasome activation

European Journal of Immunology

Volumn 43, Issue 12, 2013, Pages 3324-3335

  Gabelloni, María Laura ^a   Sabbione, Florencia ^a   Jancic, Carolina ^a,b   Bass, Juan Fuxman ^a   Keitelman, Irene ^a   Iula, Leonardo ^a   Oleastro, Matías ^c   Geffner, Jorge R ^a,b   Trevani, Analía S ^a,b  

^a ACADEMIA NACIONAL DE MEDICINA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c HOSPITAL DE PEDIATRÍA PROF DR JUAN P GARRAHAN   (Argentina)

Author keywords

Caspase 1; IL 1 ; NADPH oxidase; Neutrophil; Reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERINE PROTEINASE; CARRIER PROTEIN; IL1B PROTEIN, HUMAN; MYELOBLASTIN; NLRP3 PROTEIN, HUMAN;

ARTICLE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MACROPHAGE; NEUTROPHIL; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; CASPASE-1; CELL LINE; CLINICAL TRIAL; FEMALE; GENETICS; IL-1Β; IMMUNOLOGY; INFLAMMATION; MALE; METABOLISM; NADPH-OXIDASE; PATHOLOGY; SECRETION (PROCESS);

CASPASE-1; IL-1Β; NADPH-OXIDASE; NEUTROPHIL; REACTIVE OXYGEN SPECIES;

CARRIER PROTEINS; CASPASE 1; CELL LINE; FEMALE; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; MALE; MYELOBLASTIN; NADPH OXIDASE; REACTIVE OXYGEN SPECIES;

EID: 84894583793     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201243089     Document Type: Article

References (39)

1. Newburger, P. E., Disorders of neutrophil number and function. Hematology Am. Soc. Hematol. Educ. Program. 2006. 1: 104-110.
2. Nathan, C., Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 2006. 6: 173-182.
3. Rock, K. L., Latz, E., Ontiveros, F. and Kono, H., The sterile inflammatory response. Annu. Rev. Immunol. 2010. 28: 321-342.
4. Dinarello, C. A., Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009. 27: 519-550.
5. Hazuda, D. J., Strickler, J., Kueppers, F., Simon, P. L. and Young, P. R., Processing of precursor interleukin 1 beta and inflammatory disease. J. Biol. Chem. 1990. 265: 6318-6322.
6. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K. et al., A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 1992. 356: 768-774.
7. Franchi, L., Eigenbrod, T., Munoz-Planillo, R. and Nunez, G., The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 2009. 10: 241-247.
8. Coeshott, C., Ohnemus, C., Pilyavskaya, A., Ross, S., Wieczorek, M., Kroona, H., Leimer, A. H. et al., Converting enzyme-independent release of tumor necrosis factor alpha and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc. Natl. Acad. Sci. USA 1999. 96: 6261-6266.
9. Sugawara, S., Immune functions of proteinase 3. Crit. Rev. Immunol. 2005. 25: 343-360.
10. Tschopp, J. and Schroder, K., NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 2010. 10: 210-215.
11. Dostert, C., Petrilli, V., Van Bruggen, R., Steele, C., Mossman, B. T. and Tschopp, J., Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008. 320: 674-677.
12. Meissner, F., Molawi, K. and Zychlinsky, A., Superoxide dismutase 1 regulates caspase-1 and endotoxic shock. Nat. Immunol. 2008. 9: 866-872.
13. 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.
14. Netea, M. G., Nold-Petry, C. A., Nold, M. F., Joosten, L. A., Opitz, B., van der Meer, J. H., van de Veerdonk, F. L. et al., Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 2009. 113: 2324-2335.
15. Ekman, A. K. and Cardell, L. O., The expression and function of Nod-like receptors in neutrophils. Immunology 2010. 130: 55-63.
16. Kummer, J. A., Broekhuizen, R., Everett, H., Agostini, L., Kuijk, L., Martinon, F., van Bruggen, R. et al., Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response. J. Histochem. Cytochem. 2007. 55: 443-452.
17. Watson, R. W., Rotstein, O. D., Parodo, J., Bitar, R. and Marshall, J. C., The IL-1 beta-converting enzyme (caspase-1) inhibits apoptosis of inflammatory neutrophils through activation of IL-1 beta. J. Immunol. 1998. 161: 957-962.
18. Mankan, A. K., Dau, T., Jenne, D. and Hornung, V., The NLRP3/ASC/caspase-1 axis regulates IL-1beta processing in neutrophils. Eur. J. Immunol. 2011. 42: 710-715.
19. Joosten, L. A., Netea, M. G., Fantuzzi, G., Koenders, M. I., Helsen, M. M., Sparrer, H., Pham, C. T. et al., Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1beta. Arthritis Rheum. 2009. 60: 3651-3662.
20. Stehlik, C., Multiple interleukin-1beta-converting enzymes contribute to inflammatory arthritis. Arthritis Rheum. 2009. 60: 3524-3530.
21. Black, R. A., Kronheim, S. R., Cantrell, M., Deeley, M. C., March, C. J., Prickett, K. S., Wignall, J. et al., Generation of biologically active interleukin-1 beta by proteolytic cleavage of the inactive precursor. J. Biol. Chem. 1988. 263: 9437-9442.
22. Greten, F. R., Arkan, M. C., Bollrath, J., Hsu, L. C., Goode, J., Miething, C., Goktuna, S. I. et al., NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 2007. 130: 918-931.
23. Francois, S., El Benna, J., Dang, P. M., Pedruzzi, E., Gougerot-Pocidalo, M. A. and Elbim, C., Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J. Immunol. 2005. 174: 3633-3642.
24. Vaughan, K. R., Stokes, L., Prince, L. R., Marriott, H. M., Meis, S., Kassack, M. U., Bingle, C. D. et al., Inhibition of neutrophil apoptosis by ATP is mediated by the P2Y11 receptor. J. Immunol. 2007. 179: 8544-8553.
25. Fialkow, L., Wang, Y. and Downey, G. P., Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic. Biol. Med. 2007. 42: 153-164.
26. Hayashi, F., Means, T. K. and Luster, A. D., Toll-like receptors stimulate human neutrophil function. Blood 2003. 102: 2660-2669.
27. Holland, S. M., Chronic granulomatous disease. Clin. Rev. Allergy Immunol. 2010. 38: 3-10.
28. van de Veerdonk, F. L., Smeekens, S. P., Joosten, L. A., Kullberg, B. J., Dinarello, C. A., van der Meer, J. W. and Netea, M. G., Reactive oxygen species-independent activation of the IL-1beta inflammasome in cells from patients with chronic granulomatous disease. Proc. Natl. Acad. Sci. USA 2010. 107: 3030-3033.
29. Zhen, L., King, A. A., Xiao, Y., Chanock, S. J., Orkin, S. H. and Dinauer, M. C., Gene targeting of X chromosome-linked chronic granulomatous disease locus in a human myeloid leukemia cell line and rescue by expression of recombinant gp91phox. Proc. Natl. Acad. Sci. USA 1993. 90: 9832-9836.
30. Bauernfeind, F., Bartok, E., Rieger, A., Franchi, L., Nunez, G. and Hornung, V., Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J. Immunol. 2011. 187: 613-617.
31. Sutterwala, F. S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G. S., Grant, E. P., Bertin, J. et al., Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 2006. 24: 317-327.
32. Petrilli, V., Papin, S., Dostert, C., Mayor, A., Martinon, F. and Tschopp, J., Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 2007. 14: 1583-1589.
33. Carta, S., Tassi, S., Pettinati, I., Delfino, L., Dinarello, C. A. and Rubartelli, A., The rate of interleukin-1beta secretion in different myeloid cells varies with the extent of redox response to Toll-like receptor triggering. J. Biol. Chem. 2011. 286: 27069-27080.
34. Tassi, S., Carta, S., Vene, R., Delfino, L., Ciriolo, M. R. and Rubartelli, A., Pathogen-induced interleukin-1beta processing and secretion is regulated by a biphasic redox response. J. Immunol. 2009. 183: 1456-1462.
35. Kukulski, F., Bahrami, F., Ben Yebdri, F., Lecka, J., Martin-Satue, M., Levesque, S. A. and Sevigny, J., NTPDase1 controls IL-8 production by human neutrophils. J. Immunol. 2011. 187: 644-653.
36. Guma, M., Ronacher, L., Liu-Bryan, R., Takai, S., Karin, M. and Corr, M., Caspase 1-independent activation of interleukin-1beta in neutrophil-predominant inflammation. Arthritis Rheum. 2009. 60: 3642-3650.
37. Toldo, S., Seropian, I. M., Mezzaroma, E., Van Tassell, B. W., Salloum, F. N., Lewis, E. C., Voelkel, N. et al., Alpha-1 antitrypsin inhibits caspase-1 and protects from acute myocardial ischemia-reperfusion injury. J. Mol. Cell. Cardiol. 2011. 51: 244-251.
38. Nauseef, W. M., Isolation of human neutrophils from venous blood. Methods Mol. Biol. 2007. 412: 15-20.
39. Dinarello, C. A., Muegge, K. and Durum, S. K., Measurement of soluble and membrane-bound interleukin 1 using a fibroblast bioassay. Curr. Protoc. Immunol. 2001. 6.2.1-6.2.7.