Pneumolysin activates neutrophil extracellular trap formation

Clinical and Experimental Immunology

Volumn 184, Issue 3, 2016, Pages 358-367

  Nel, J G ^a   Theron, A J ^b   Durandt, C ^b   Tintinger, G R ^b   Pool, R ^a   Mitchell, T J ^c   Feldman, C ^d   Anderson, R ^b  

^a Department of Haematology ^*  (South Africa)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Calcium; Chronic granulomatous disease; NETosis; Neutrophils; Pneumolysin; Reactive oxygen species; Toll like receptor 4

Indexed keywords

CALCIUM ION; CELL DNA; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; DNA FRAGMENT; HISTONE; MYELOPEROXIDASE; PNEUMOLYSIN; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 4; 4',6 DIAMIDINO 2 PHENYLINDOLE; BACTERIAL PROTEIN; CITRULLINE; DNA; INDOLE DERIVATIVE; MONOCLONAL ANTIBODY; PEROXIDASE; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; RECOMBINANT PROTEIN; STREPTOLYSIN; TLR4 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; EXTRACELLULAR TRAP; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IN VITRO STUDY; LEUKOCYTE ACTIVATION; NEUTROPHIL; NORMAL HUMAN; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; SPECTROFLUOROMETRY; AGONISTS; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; PRIMARY CELL CULTURE; SECRETION (PROCESS); STREPTOCOCCUS PNEUMONIAE;

ANTIBODIES, MONOCLONAL; BACTERIAL PROTEINS; CELL SURVIVAL; CITRULLINE; DNA; EXTRACELLULAR TRAPS; GENE EXPRESSION; HISTONES; HUMANS; INDOLES; NEUTROPHILS; PEROXIDASE; PRIMARY CELL CULTURE; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS; TOLL-LIKE RECEPTOR 4;

EID: 84968898658     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12766     Document Type: Article

References (46)

1. Steel HC, Cockeran R, Anderson R, Feldman C. Overview of community-acquired pneumonia and the role of inflammatory mechanisms in the immunopathogenesis of severe pneumococcal disease. Mediators Inflamm 2013; 2013:490346.
2. Welte T, Torres A, Nathwani D. Clinical and economic burden of community-acquired pneumonia among adults in Europe. Thorax 2012; 67:71-9.
3. Feldman C, Anderson R. Review: current and new generation pneumococcal vaccines. J Infect 2014; 69:309-25.
4. Aliberti S, Ramirez JA. Cardiac diseases complicating community-acquired pneumonia. Curr Opin Infect Dis 2014; 27:295-301.
5. Feldman C, Munro NC, Jeffery PK et al. Pneumolysin induces the salient histologic features of pneumococcal infection in the rat lung in vivo. Am J Respir Cell Mol Biol 1991; 5:416-23.
6. Witzenrath M, Gutbier B, Hocke AC et al. Role of pneumolysin for the development of acute lung injury in pneumococcal pneumonia. Crit Care Med 2006; 34:1947-54.
7. Garcia-Suarez Mdel M, Florez N, Astudillo A et al. The role of pneumolysin in mediating lung damage in a lethal pneumococcal pneumonia murine model. Respir Res 2007; 8:3.
8. Malley R, Henneke P, Morse SC et al. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci USA 2003; 100:1966-71.
9. Musher DM, Rueda AM, Kaka AS, Mapara SM. The association between pneumococcal pneumonia and acute cardiac events. Clin Infect Dis 2007; 45:158-65.
10. Corrales-Medina VF, Madjid M, Musher DM. Role of acute infection in triggering acute coronary syndromes. Lancet Infect Dis 2010; 10:83-92.
11. Corrales-Medina VF, Musher DM, Wells GA, Chirinos JA, Chen L, Fine MJ. Cardiac complications in patients with community-acquired pneumonia: incidence, timing, risk factors, and association with short-term mortality. Circulation 2012; 125:773-81.
12. Alhamdi Y, Neill DR, Abrams ST et al. Circulating pneumolysin is a potent inducer of cardiac injury during pneumococcal infection. PLOS Pathog 2015; 11:e1004836.
13. Brown AO, Mann B, Gao G et al. Streptococcus pneumoniae translocates into the myocardium and forms unique microlesions that disrupt cardiac function. PLOS Pathog 2014; 10:e1004383.
14. Mangold A, Alias S, Scherz T et al. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res 2015; 116:1182-92.
15. Borissoff JI, ten Cate H. From neutrophil extracellular traps release to thrombosis: an overshooting host-defense mechanism? J Thromb Haemost 2011; 9:1791-4.
16. Narayana Moorthy A, Narasaraju T, Rai P et al. In vivo and in vitro studies on the roles of neutrophil extracellular traps during secondary pneumococcal pneumonia after primary pulmonary influenza infection. Front Immunol 2013; 4:56.
17. Ward PA, Grailer JJ. Acute lung injury and the role of histones. Transl Respir Med 2014; 2:1.
18. Stakos DA, Kambas K, Konstantinidis T et al. Expression of functional tissue factor by neutrophil extracellular traps in culprit artery of acute myocardial infarction. Eur Heart J 2015; 36:1405-14.
19. Robb CT, Dyrynda EA, Gray RD, Rossi AG, Smith VJ. Invertebrate extracellular phagocyte traps show that chromatin is an ancient defence weapon. Nat Commun 2014; 5:4627.
20. Brinkmann V, Reichard U, Goosmann C et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532-5.
21. Saffarzadeh M, Juenemann C, Queisser MA et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLOS ONE 2012; 7:e32366.
22. Saunders FK, Mitchell TJ, Walker JA, Andrew PW, Boulnois GJ. Pneumolysin, the thiol-activated toxin of Streptococcus pneumoniae, does not require a thiol group for in vitro activity. Infect Immun 1989; 57:2547-52.
23. Kirkham LA, Kerr AR, Douce GR et al. Construction and immunological characterization of a novel nontoxic protective pneumolysin mutant for use in future pneumococcal vaccines. Infect Immun 2006; 74:586-93.
24. Cockeran R, Theron AJ, Steel HC et al. Proinflammatory interactions of pneumolysin with human neutrophils. J Infect Dis 2001; 183:604-11.
25. Cockeran R, Steel HC, Mitchell TJ, Feldman C, Anderson R. Pneumolysin potentiates production of prostaglandin E(2) and leukotriene B(4) by human neutrophils. Infect Immun 2001; 69:3494-6.
26. Berkes E, Oehmke F, Tinneberg HR, Preissner KT, Saffarzadeh M. Association of neutrophil extracellular traps with endometriosis-related chronic inflammation. Eur J Obstet Gynecol Reprod Biol 2014; 183:193-200.
27. Desjardins P, Conklin D. NanoDrop microvolume quantitation of nucleic acids. J Vis Exp 2010, doi:10.3791/2565.
28. Cockeran R, Steel HC, Theron AJ, Mitchell TJ, Feldman C, Anderson R. Characterization of the interactions of the pneumolysoid, Delta6 PLY, with human neutrophils in vitro. Vaccine 2011; 29:8780-2.
29. Tintinger GR, Theron AJ, Steel HC, Anderson R. Accelerated calcium influx and hyperactivation of neutrophils in chronic granulomatous disease. Clin Exp Immunol 2001; 123:254-63.
30. Barrientos L, Marin-Esteban V, de Chaisemartin L et al. An improved strategy to recover large fragments of functional human neutrophil extracellular traps. Front Immunol 2013; 4:166.
31. Spreer A, Kerstan H, Bottcher T et al. Reduced release of pneumolysin by Streptococcus pneumoniae in vitro and in vivo after treatment with nonbacteriolytic antibiotics in comparison to ceftriaxone. Antimicrob Agents Chemother 2003; 47:2649-54.
32. Mongardon N, Max A, Bougle A et al. Epidemiology and outcome of severe pneumococcal pneumonia admitted to intensive care unit: a multicenter study. Crit Care 2012; 16:R155.
33. Pilsczek FH, Salina D, Poon KK et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 2010; 185:7413-25.
34. Parker H, Dragunow M, Hampton MB, Kettle AJ, Winterbourn CC. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J Leukoc Biol 2012; 92:841-9.
35. Scapini P, Cassatella MA. Social networking of human neutrophils within the immune system. Blood 2014; 124:710-9.
36. Mitchell TJ, Dalziel CE. The biology of pneumolysin. Subcell Biochem 2014; 80:145-60.
37. Wolfmeier H, Schoenauer R, Atanassoff AP et al. Ca(2)(+)-dependent repair of pneumolysin pores: a new paradigm for host cellular defense against bacterial pore-forming toxins. Biochim Biophys Acta 2015; 1853:2045-54.
38. Rada B, Jendrysik MA, Pang L et al. Pyocyanin-enhanced neutrophil extracellular trap formation requires the NADPH oxidase. PLOS ONE 2013; 8:e54205.
39. Arai Y, Nishinaka Y, Arai T et al. Uric acid induces NADPH oxidase-independent neutrophil extracellular trap formation. Biochem Biophys Res Commun 2014; 443:556-61.
40. Kadioglu A, Andrew PW. The innate immune response to pneumococcal lung infection: the untold story. Trends Immunol 2004; 25:143-9.
41. Mori Y, Yamaguchi M, Terao Y, Hamada S, Ooshima T, Kawabata S. Alpha-Enolase of Streptococcus pneumoniae induces formation of neutrophil extracellular traps. J Biol Chem 2012; 287:10472-81.
42. Wartha F, Beiter K, Albiger B et al. Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol 2007; 9:1162-71.
43. Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A, Henriques-Normark B. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 2006; 16:401-7.
44. Anderson R, Steel HC, Cockeran R et al. Comparison of the effects of macrolides, amoxicillin, ceftriaxone, doxycycline, tobramycin and fluoroquinolones, on the production of pneumolysin by Streptococcus pneumoniae in vitro. J Antimicrob Chemother 2007; 60:1155-8.
45. Henry BD, Neill DR, Becker KA et al. Engineered liposomes sequester bacterial exotoxins and protect from severe invasive infections in mice. Nat Biotechnol 2015; 33:81-8.
46. Bozdag M, Dreker T, Henry C et al. Novel small molecule protein arginine deiminase 4 (PAD4) inhibitors. Bioorg Med Chem Lett 2013; 23:715-9.