Understanding the entanglement: Neutrophil extracellular traps (NETs) in cystic fibrosis

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue APR, 2017, Pages

  Martínez Alemán, Saira R ^a   Campos García, Lizbeth ^a   Palma Nicolas, José P ^a   Hernández Bello, Romel ^a   González, Gloria M ^a   Sánchez González, Alejandro ^a  

^a Medicina UANL   (Mexico)

Author keywords

Burkholderia cepacia; CFTR; Cystic fibrosis; NETs; Neutrophil; Pseudomonas aeruginosa; Staphylococcus aureus

Indexed keywords

CALGRANULIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ZINC ION;

ACHROMOBACTER XYLOSOXIDANS; ARTICLE; ASPERGILLOSIS; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BIOFILM; BURKHOLDERIA CEPACIA; CANDIDA ALBICANS; CELL DEATH; CYSTIC FIBROSIS; DISEASE EXACERBATION; EXTRACELLULAR TRAP; FUNGUS GROWTH; GENE MUTATION; HOST PATHOGEN INTERACTION; HUMAN; NEUTROPHIL; NONHUMAN; PANDORAEA; PHAGOCYTOSIS; PSEUDOMONAS AERUGINOSA; RESPIRATORY FUNCTION; RESPIRATORY TRACT INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; STENOTROPHOMONAS MALTOPHILIA; STREPTOCOCCUS; BACTERIUM; COMPLICATION; IMMUNOLOGY; MICROBIOLOGY; MIXED INFECTION; NEUTROPHIL CHEMOTAXIS; PATHOLOGY;

BACTERIA; BACTERIAL INFECTIONS; COINFECTION; CYSTIC FIBROSIS; EXTRACELLULAR TRAPS; HUMANS; NEUTROPHIL INFILTRATION;

EID: 85027510731     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00104     Document Type: Article

References (68)

1. Aimanianda, V., Bayry, J., Bozza, S., Kniemeyer, O., Perruccio, K., Elluru, S. R., et al. (2009). Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460, 1117–1121. doi: 10.1038/nature08264
2. Amulic, B., Cazalet, C., Hayes, G. L., Metzler, K. D., and Zychlinsky, A. (2012). Neutrophil function: from mechanisms to disease. Annu. Rev. Immunol. 30, 459–489. doi: 10.1146/annurev-immunol-020711-074942
3. Armstead, J., Morris, J., and Denning, D. W. (2014). Multi-country estimate of different manifestations of aspergillosis in cystic fibrosis. PLoS ONE 9:e98502. doi: 10.1371/journal.pone.0098502
4. Bergsson, G., Reeves, E. P., McNally, P., Chotirmall, S. H., Greene, C. M., Greally, P., et al. (2009). LL-37 complexation with glycosaminoglycans in cystic fibrosis lungs inhibits antimicrobial activity, which can be restored by hypertonic saline. J. Immunol. 183, 543–551. doi: 10.4049/jimmunol.0803959
5. Besier, S., Smaczny, C., Von Mallinckrodt, C., Krahl, A., Ackermann, H., Brade, V., et al. (2007). Prevalence and clinical significance of Staphylococcus aureus smallcolony variants in cystic fibrosis lung disease. J. Clin. Microbiol. 45, 168–172. doi: 10.1128/JCM.01510-06
6. Borregaard, N., and Cowland, J. B. (1997). Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89, 3503–3521.
7. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532–1535. doi: 10.1126/science.1092385
8. Brinkmann, V., and Zychlinsky, A. (2012). Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol. 198, 773–783. doi: 10.1083/jcb.201203170
9. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., et al. (2010). Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog. 6:e1000873. doi: 10.1371/journal.ppat.1000873
10. Callaghan, M., and McClean, S. (2012). Bacterial host interactions in cystic fibrosis. Curr. Opin. Microbiol. 15, 71–77. doi: 10.1016/j.mib.2011.11.001
11. Chotirmall, S. H., and McElvaney, N. G. (2014). Fungi in the cystic fibrosis lung: bystanders or pathogens? Int. J. Biochem. Cell Biol. 52, 161–173. doi: 10.1016/j.biocel.2014.03.001
12. Cullen, L., and McClean, S. (2015). Bacterial adaptation during chronic respiratory infections. Pathogens 4, 66–89. doi: 10.3390/pathogens4010066
13. Cutting, G. R. (2015). Cystic fibrosis genetics: from molecular understanding to clinical application. HHS Public Access 16, 45–56. doi: 10.1038/nrg3849
14. Dubois, A. V., Gauthier, A., Bréa, D., Varaigne, F., Diot, P., Gauthier, F., et al. (2012). Influence of DNA on the activities and inhibition of neutrophil serine proteases in cystic fibrosis sputum. Am. J. Respir. Cell Mol. Biol. 47, 80–86. doi: 10.1165/rcmb.2011-0380OC
15. Dwyer, M., Shan, Q., D'Ortona, S., Maurer, R., Mitchell, R., Olesen, H., et al. (2014). Cystic fibrosis sputum DNA has NETosis characteristics and neutrophil extracellular trap release is regulated by macrophage migration-inhibitory factor. J. Innate Immun. 6, 765–779. doi: 10.1159/000363242
16. Eisele, N. A., and Anderson, D. M. (2011). Host defense and the airway epithelium: frontline responses that protect against bacterial invasion and pneumonia. J. Pathog. 2011:249802. doi: 10.4061/2011/249802
17. Filkins, L. M., and O'Toole, G. A. (2015). Cystic fibrosis lung infections: polymicrobial, complex, and hard to treat. PLoS Pathog. 11:e1005258. doi: 10.1371/journal.ppat.1005258
18. Folescu, T. W., da Costa, C. H., Cohen, R. W. F., da Conceição Neto, O. C., Albano, R. M., and Marques, E. A. (2015). Burkholderia cepacia complex: clinical course in cystic fibrosis patients. BMC Pulm. Med. 15:158. doi: 10.1186/s12890-015-0148-2
19. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231–241. doi: 10.1083/jcb.200606027
20. Gan, K. H., Veeze, H. J., van den Ouweland, A. M., Halley, D. J., Scheffer, H., van der Hout, A., et al. (1995). A cystic fibrosis mutation associated with mild lung disease. N. Engl. J. Med. 333, 95–99.
21. Genestier, A. L., Michallet, M. C., Prévost, G., Bellot, G., Chalabreysse, L., Peyrol, S., et al. (2005). Staphylococcus aureus Panton-Valentine leucocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J. Clin. Invest. 115, 3117–3127. doi: 10.1172/JCI22684
22. Gilligan, P. H. (2014). Infections in patients with cystic fibrosis: diagnostic microbiology update. Clin. Lab. Med. 34, 197–217. doi: 10.1016/j.cll.2014.02.001
23. Gray, R., McCullagh, B., and McCray, P. (2015). NETs and CF lung disease: current status and future prospects. Antibiotics 4, 62–75. doi: 10.3390/antibiotics4010062
24. Halverson, T. W. R., Wilton, M., Poon, K. K. H., Petri, B., and Lewenza, S. (2015). DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog. 11:e1004593. doi: 10.1371/journal.ppat.1004593
25. Hirschfeld, J., Dommisch, H., Skora, P., Horvath, G., Latz, E., Hoerauf, A., et al. (2015). Neutrophil extracellular trap formation in supragingival biofilms. Int. J. Med. Microbiol. 305, 453–463. doi: 10.1016/j.ijmm.2015.04.002
26. Hubert, D., Réglier-Poupet, H., Sermet-Gaudelus, I., Ferroni, A., Le Bourgeois, M., Burgel, P. R., et al. (2013). Association between Staphylococcus aureus alone or combined with Pseudomonas aeruginosa and the clinical condition of patients with cystic fibrosis. J. Cystic Fibros. 12, 497–503. doi: 10.1016/j.jcf.2012.12.003
27. Johnson, L., Horsman, S. R., Charron-Mazenod, L., Turnbull, A. L., Mulcahy, H., Surette, M. G., et al. (2013). Extracellular DNA-induced antimicrobial peptide resistance in Salmonella enterica serovar Typhimurium. BMC Microbiol. 13:115. doi: 10.1186/1471-2180-13-115
28. Johnson, L., Mulcahy, H., Kanevets, U., Shi, Y., and Lewenza, S. (2012). Surfacelocalized spermidine protects the Pseudomonas aeruginosa: outer membrane from antibiotic treatment and oxidative stress. J. Bacteriol. 194, 813–826. doi: 10.1128/JB.05230-11
29. Juneau, R. A., Pang, B., Weimer, K. W. D., Armbruster, C. E., and Swords, W. E. (2011). Nontypeable Haemophilus influenzae initiates formation of neutrophil extracellular traps. Infect. Immun. 79, 431–438. doi: 10.1128/IAI. 00660-10
30. Kirchner, K. K., Wagener, J. S., Khan, T. Z., Copenhaver, S. C., and Accurso, F. J. (1996). Increased DNA levels in bronchoalveolar lavage fluid obtained from infants with cystic fibrosis. Am. J. Respir. Crit. Care Med. 154, 1426–1429. doi: 10.1164/ajrccm.154.5.8912759
31. Klebanoff, S. J., Kinsella, M. G., and Wightt, T. N. (1993). Degradation of endothelial cell matrix heparan sulfate proteoglycan by elastase and the myeloperoxidase-H202-chloride system. Am. J. Pathol. 143, 907–917.
32. Kolaczkowska, E., and Kubes, P. (2013). Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175. doi: 10.1038/nri3399
33. Leshner, M., Wang, S., Lewis, C., Zheng, H., Chen, X. A., Santy, L., et al. (2012). PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Front. Immunol. 3:307. doi: 10.3389/fimmu.2012.00307
34. LiPuma, J. J. (2010). The changing microbial epidemiology in cystic fibrosis. Clin. Microbiol. Rev. 23, 299–323. doi: 10.1128/CMR.00068-09
35. Lu, T., Kobayashi, S. D., Quinn, M. T., and DeLeo, F. R. (2012). A NET outcome. Front. Immunol. 3:365 doi: 10.3389/fimmu.2012.00365
36. Manzenreiter, R., Kienberger, F., Marcos, V., Schilcher, K., Krautgartner, W. D., Obermayer, A., et al. (2012). Ultrastructural characterization of cystic fibrosis sputum using atomic force and scanning electron microscopy. J. Cystic Fibros. 11, 84–92. doi: 10.1016/j.jcf.2011.09.008
37. Marcos, V., Zhou-Suckow, Z., Önder Yildirim, A., Bohla, A., Hector, A., Vitkov, L., et al. (2015). Free DNA in cystic fibrosis airway fluids correlates with airflow obstruction. Mediators Inflamm. 2015:408935. doi: 10.1155/2015/408935
38. McCormick, A., Heesemann, L., Wagener, J., Marcos, V., Hartl, D., Loeffler, J., et al. (2010). NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microb. Infect. 12, 928–936. doi: 10.1016/j.micinf.2010.06.009
39. Menestrina, G., Dalla Serra, M., Comai, M., Coraiola, M., Viero, G., Werner, S., et al. (2003). Ion channels and bacterial infection: the case of β-barrel pore-forming protein toxins of Staphylococcus aureus. FEBS Lett. 552, 54–60. doi: 10.1016/S0014-5793(03)00850-0
40. Mulcahy, H., Charron-Mazenod, L., and Lewenza, S. (2008). Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4:e1000213. doi: 10.1371/journal.ppat.1000213
41. Neeli, I., Khan, S. N., and Radic, M. (2008). Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol. 180, 1895–1902. doi: 10.4049/jimmunol.180.3.1895
42. O'Sullivan, B. P., and Freedman, S. D. (2009). Cystic fibrosis. Lancet 373, 1891–1904. doi: 10.1016/S0140-6736(09)60327-5
43. Painter, R. G., Bonvillain, R. W., Valentine, V. G., Lombard, G. A., LaPlace, S. G., Nauseef, W. M., et al. (2008). The role of chloride anion and CFTR in killing of Pseudomonas aeruginosa by normal and CF neutrophils. J. Leukoc. Biol. 83, 1345–1353. doi: 10.1189/jlb.0907658
44. Papayannopoulos, V., Metzler, K. D., Hakkim, A., and Zychlinsky, A. (2010). Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191, 677–691. doi: 10.1083/jcb.201006052
45. Papayannopoulos, V., Staab, D., and Zychlinsky, A. (2011). Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving dnase therapy. PLoS ONE 6:e28526. doi: 10.1371/journal.pone.0028526
46. Papayannopoulos, V., and Zychlinsky, A. (2009). NETs: a new strategy for using old weapons. Trends Immunol. 30, 513–521. doi: 10.1016/j.it.2009.07.011
47. Pilsczek, F. H., Salina, D., Poon, K. K., Fahey, C., Yipp, B. G., Sibley, C. D., et al. (2010). A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J. Immunol. 185, 7413–7425. doi: 10.4049/jimmunol.1000675
48. Rahman, S., and Gadjeva, M. (2014). Does NETosis contribute to the bacterial pathoadaptation in cystic fibrosis? Front. Immunol. 5:378. doi: 10.3389/fimmu.2014.00378
49. Ratjen, F., Paul, K., van Koningsbruggen, S., Breitenstein, S., Rietschel, E., and Nikolaizik, W. (2005). DNA concentrations in BAL fluid of cystic fibrosis patients with early lung disease: influence of treatment with dornase alpha. Pediatr. Pulmonol. 39, 1–4. doi: 10.1002/ppul.20134
50. Rochael, N. C., Guimarães-Costa, A. B., Nascimento, M. T. C., DeSouza-Vieira, T. S., Oliveira, M. P., Garcia e Souza, L. F., et al. (2015). Classical ROS-dependent and early/rapid ROS-independent release of Neutrophil Extracellular Traps triggered by Leishmania parasites. Sci. Rep. 5:18302. doi: 10.1038/srep18302
51. Rogan, M. P., Taggart, C. C., Greene, C. M., Murphy, P. G., O'Neill, S. J., and McElvaney, N. G. (2004). Loss of microbicidal activity and increased formation of biofilm due to decreased lactoferrin activity in patients with cystic fibrosis. J. Infect. Dis. 190, 1245–1253. doi: 10.1086/423821
52. Rowe, S.M., Miller, S., and Sorscher, E.J. (2005). Cystic fibrosis. N. Engl. J. Med. 352, 1992–2001. doi: 10.1056/NEJMra043184
53. Saffarzadeh, M., Juenemann, C., Queisser, M. A., Lochnit, G., Barreto, G., Galuska, S. P., et al. (2012). Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS ONE 7:e32366. doi: 10.1371/journal.pone.0032366
54. Sagel, S. D., Sontag, M. K., Accurso, F. J., Bergsson, G., Reeves, E. P., McNally, P., et al. (2004). Relationship between antimicrobial proteins and airway inflammation and infection in cystic fibrosis. Pediatr. Pulmonol. 44, 402–409. doi: 10.1002/ppul.21028
55. Saiman, L., Cacalano, G., and Prince, A. (1990). Pseudomonas cepacia adherence to respiratory epithelial cells is enhanced by Pseudomonas aeruginosa. Infect. Immun. 58, 2578–2584.
56. Sohnle, P. G., Hahn, B. L., and Santhanagopalan, V. (1996). Inhibition of Candida albicans growth by calprotectin in the absence of direct contact with the organisms. J. Infect. Dis. 174, 1369–1372. doi: 10.1093/infdis/174.6.1369
57. Thammavongsa, V., Missiakas, D., and Schneewind, O. (2013). Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science 342, 863–866. doi: 10.1126/science.1242255
58. Urban, C. F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., et al. (2009). Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5:e1000639. doi: 10.1371/journal.ppat.1000639
59. Urban, C. F., Reichard, U., Brinkmann, V., and Zychlinsky, A. (2006). Neutrophil extracellular traps capture and kill Candida albicans and hyphal forms. Cell. Microbiol. 8, 668–676. doi: 10.1111/j.1462-5822.2005.00659.x
60. Voyich, J. M., Braughton, K. R., Sturdevant, D. E., Whitney, A. R., Saïd-Salim, B., Porcella, S. F., et al. (2005). Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175, 3907–3919. doi: 10.4049/jimmunol.175.6.3907
61. Wakeman, C. A., Moore, J. L., Noto, M. J., Zhang, Y., Singleton, M. D., Prentice, B. M., et al. (2016). The innate immune protein calprotectin promotes Pseudomonas aeruginosa and Staphylococcus aureus interaction. Nat. Commun. 7:11951. doi: 10.1038/ncomms11951
62. Wang, Y., Li, M., Stadler, S., Correll, S., Li, P., Wang, D., et al. (2009). Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205–213. doi: 10.1083/jcb.200806072
63. Welsh, M. J., and Smith, A. E. (1993). Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 73, 1251–1254. doi: 10.1016/0092-8674(93)90353-R
64. Winstanley, C., O'Brien, S., and Brockhurst, M. A. (2016). Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol. 24, 327–337. doi: 10.1016/j.tim.2016.01.008
65. Yipp, B. G., and Kubes, P. (2016). Review Article NETosis : how vital is it? Blood 122, 2784–2795. doi: 10.1182/blood-2013-04-457671
66. Young, R. L., Malcolm, K. C., Kret, J. E., Caceres, S. M., Poch, K. R., Nichols, D. P., et al. (2011). Neutrophil extracellular trap (NET)-mediated killing of Pseudomonas aeruginosa: evidence of acquired resistance within the CF airway, independent of CFTR. PLoS ONE 6:e23637. doi: 10.1371/journal.pone.0023637
67. Zawrotniak, M., and Rapala-Kozik, M. (2013). Neutrophil extracellular traps (NETs) - formation and implications. Acta Biochim. Pol. 60, 277–284.
68. Zemanick, E. T., Sagel, S. D., and Harris, J. K. (2011). The airway microbiome in cystic fibrosis and implications for treatment. Curr. Opin. Pediatr. 23, 319–324. doi: 10.1097/MOP.0b013e32834604f2