Neutrophil extracellular traps can serve as platforms for processing and activation of IL-1 family cytokines

FEBS Journal

Volumn 284, Issue 11, 2017, Pages 1712-1725

  Clancy, Danielle M ^a   Henry, Conor M ^a   Sullivan, Graeme P ^a   Martin, Seamus J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

cathepsin G; elastase; IL 1 family; IL 1 , IL 36; inflammation; NETs; neutrophil extracellular traps; protease

Indexed keywords

CATHEPSIN G; ELASTASE; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 36ALPHA; INTERLEUKIN 36BETA; INTERLEUKIN 36GAMMA; MYELOBLASTIN; UNCLASSIFIED DRUG; CTSG PROTEIN, HUMAN; DEOXYRIBONUCLEASE I; IL36G PROTEIN, HUMAN; INTERLEUKIN 36, HUMAN; LEUKOCYTE ELASTASE; PHORBOL 13 ACETATE 12 MYRISTATE; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DEGRANULATION; ENZYME ACTIVITY; EXTRACELLULAR SPACE; EXTRACELLULAR TRAP; HELA CELL LINE; HUMAN; HUMAN CELL; INFLAMMATION; PRIORITY JOURNAL; BLOOD; CELL GRANULE; DRUG EFFECTS; ENZYMOLOGY; LEUKOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY;

CATHEPSIN G; CYTOPLASMIC GRANULES; DEOXYRIBONUCLEASE I; EXTRACELLULAR TRAPS; HUMANS; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-1ALPHA; LEUKOCYTE ELASTASE; MYELOBLASTIN; NEUTROPHIL ACTIVATION; RECOMBINANT PROTEINS; TETRADECANOYLPHORBOL ACETATE;

EID: 85018942401     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.14075     Document Type: Article

References (46)

1. Amulic B, Cazalet C, Hayes GL, Metzler KD & Zychlinsky A (2012) Neutrophil function: from mechanisms to disease. Annu Rev Immunol 30, 459–489.
2. Kolaczkowska E & Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13, 159–175.
3. Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23, 197–223.
4. Pham CT (2008) Neutrophil serine proteases fine-tune the inflammatory response. Int J Biochem Cell Biol 40, 1317–1333.
5. Borregaard N, Sorensen OE & Theilgaard-Monch K (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol 28, 340–345.
6. Tecchio C, Micheletti A & Cassatella MA (2014) Neutrophil-derived cytokines: facts beyond expression. Front Immunol 5, 508.
7. Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, Luthi AU, Reeves EP, McElvaney NG, Medema JP, Lavelle EC et al. (2011) Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1alpha. Mol Cell 44, 265–278.
8. Lefrancais E, Roga S, Gautier V, Gonzalez-de-Peredo A, Monsarrat B, Girard JP & Cayrol C (2012) IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc Natl Acad Sci USA 109, 1673–1678.
9. Afonina IS, Muller C, Martin SJ & Beyaert R (2015) Proteolytic processing of interleukin-1 family cytokines: variations on a common theme. Immunity 42, 991–1004.
10. Henry CM, Sullivan GP, Clancy DM, Afonina IS, Kulms D & Martin SJ (2016) Neutrophil-derived proteases escalate inflammation through activation of IL-36 family cytokines. Cell Rep 14, 708–722.
11. Martin SJ (2016) Cell death and inflammation: the case for IL-1 family cytokines as the canonical DAMPs of the immune system. FEBS J 283, 2599–2615.
12. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y & Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532–1535.
13. Yousefi S, Mihalache C, Kozlowski E, Schmid I & Simon HU (2009) Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 16, 1438–1444.
14. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC et al. (2012) Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 18, 1386–1393.
15. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V & Zychlinsky A (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176, 231–241.
16. Papayannopoulos V & Zychlinsky A (2009) NETs: a new strategy for using old weapons. Trends Immunol 30, 513–521.
17. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR & Zychlinsky A (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5, e1000639.
18. Brinkmann V & Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198, 773–783.
19. Branzk N & Papayannopoulos V (2013) Molecular mechanisms regulating NETosis in infection and disease. Semin Immunopathol 35, 513–530.
20. Halverson TW, Wilton M, Poon KK, Petri B & Lewenza S (2015) DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog 11, e1004593.
21. Brinkmann V, Laube B, Abu Abed U, Goosmann C & Zychlinsky A (2010) Neutrophil extracellular traps: how to generate and visualize them. J Vis Exp 24, pii: 1724, doi: 10.3791/1724.
22. Papayannopoulos V, Metzler KD, Hakkim A & Zychlinsky A (2010) Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 191, 677–691.
23. Johnston A, Xing X, Guzman AM, Riblett M, Loyd CM, Ward NL, Wohn C, Prens EP, Wang F, Maier LE et al. (2011) IL-1F5, -F6, -F8, and -F9: a novel IL-1 family signaling system that is active in psoriasis and promotes keratinocyte antimicrobial peptide expression. J Immunol 186, 2613–2622.
24. D'Erme AM, Wilsmann-Theis D, Wagenpfeil J, Holzel M, Ferring-Schmitt S, Sternberg S, Wittmann M, Peters B, Bosio A, Bieber T et al. (2015) IL-36gamma (IL-1F9) is a biomarker for psoriasis skin lesions. J Invest Dermatol 135, 1025–1032.
25. Towne JE, Renshaw BR, Douangpanya J, Lipsky BP, Shen M, Gabel CA & Sims JE (2011) Interleukin-36 (IL-36) ligands require processing for full agonist (IL-36alpha, IL-36beta, and IL-36gamma) or antagonist (IL-36Ra) activity. J Biol Chem 286, 42594–42602.
26. Clancy DM, Henry CM, Davidovich PB, Sullivan GP, Belotcerkovskaya E & Martin SJ (2016) Production of biologically active IL-36 family cytokines through insertion of N-terminal caspase cleavage motifs. FEBS Open Bio 6, 338–348.
27. Kasperkiewicz P, Poreba M, Snipas SJ, Parker H, Winterbourn CC, Salveson GS & Drag M (2014) Design of ultrasensitive probes for human neutrophil elastase through hybrid combinatorial substrate library profiling. Proc Natl Acad Sci USA 111, 2518–2523.
28. Menegazzi R, Decleva E & Dri P (2012) Killing by neutrophil extracellular traps: fact or folklore? Blood 119, 1214–1216.
29. Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A & Henriques-Normark B (2006) An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16, 401–407.
30. Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, 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.
31. Chen CJ, Kono H, Golenbock D, Reed G, Akira S & Rock KL (2007) Identification of a key pathway required for sterile inflammatory response triggered by dying cells. Nat Med 13, 851–856.
32. Rider P, Carmi Y, Guttman O, Braiman A, Cohen I, Voronov E, White MR, Dinarello CA & Apte RN (2011) IL-1α and IL-1β recruit different myeloid cells and promote different stages of sterile inflammation. J Immunol 187, 4835–4843.
33. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z, Grone HJ, Brinkmann V & Jenne DE (2009) Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 15, 623–625.
34. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, Herrmann M, Voll RE & Zychlinsky A (2010) Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA 107, 9813–9818.
35. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, Gizinski A, Yalavarthi S, Knight JS, Friday S, Li S, Patel RM, Subramanian V et al. (2013) NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 5, 178ra40.
36. Barnado A, Crofford LJ & Oates CJ (2016) At the Bedside: neutrophil extracellular traps (NETs) as targets for biomarkers and therapies in autoimmune diseases. J Leukoc Biol 99, 265–278.
37. Kaplan MJ & Radic M (2012) Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 189, 2689–2695.
38. Terui T, Ozawa M & Tagami H (2000) Role of neutrophils in induction of acute inflammation in T-cell-mediated immune dermatosis, psoriasis: a neutrophil-associated inflammation-boosting loop. Exp Dermatol 9, 1–10.
39. Murphy M, Kerr P & Grant-Kels JM (2007) The histopathologic spectrum of psoriasis. Clin Dermatol 25, 524–528.
40. Nestle FO, Kaplan DH & Barker J (2009) Psoriasis. N Engl J Med 361, 496–508.
41. Towne JE & Sims JE (2012) IL-36 in psoriasis. Curr Opin Pharmacol 12, 486–490.
42. Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, Villanueva EC, Shah P, Kaplan MJ & Bruce AT (2011) Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 187, 490–500.
43. Korkmaz B, Moreau T & Gauthier F (2008) Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions. Biochimie 90, 27–242.
44. Netea MG, van de Veerdonk FL, van der Meer JW, Dinarello CA & Joosten LA (2015) Inflammasome-independent regulation of IL-1-family cytokines. Ann Rev Immunol 33, 49–77.
45. Hu SC, Yu HS, Yen FL, Lin CL, Chen GS & Lan CC (2016) Neutrophil extracellular trap formation is increased in psoriasis and induces human β-defensin-2 production in epidermal keratinocytes. Sci Rep 6, 31119.
46. Haslett C, Gurthrie LA, Kopaniak MM, Johnston RB Jr & Henson PM (1985) Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharides. Am J Pathol 119, 101–110.