Delayed neutrophil apoptosis enhances NET formation in cystic fibrosis

Thorax

Volumn 73, Issue 2, 2018, Pages 134-144

  Gray, Robert D ^a   Hardisty, Gareth ^a   Regan, Kate H ^a   Smith, Maeve ^a   Robb, Calum T ^a   Duffin, Rodger ^a   MacKellar, Annie ^a   Felton, Jennifer M ^a   Paemka, Lily ^b   McCullagh, Brian N ^b   Lucas, Christopher D ^a   Dorward, David A ^a   McKone, Edward F ^c   Cooke, Gordon ^d   Donnelly, Seamas C ^d   Singh, Pradeep K ^e   Stoltz, David A ^b   Haslett, Christopher ^a   McCray, Paul B ^b   Whyte, Moira K B ^a   Rossi, Adriano G ^a   Davidson, Donald J ^a   more..

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF IOWA   (United States)

^c ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^d TRINITY COLLEGE DUBLIN   (Ireland)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cystic Fibrosis; Neutrophil Biology

Indexed keywords

CYCLIN DEPENDENT KINASE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; IVACAFTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CHANNEL GATING; CONTROLLED STUDY; CYSTIC FIBROSIS; EXTRACELLULAR TRAP; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MACROPHAGE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; ADULT; ANIMAL; BLOOD; CASE CONTROL STUDY; IMMUNOLOGY; PATHOLOGY; PHYSIOLOGY; PIG; TIME FACTOR;

ADULT; ANIMALS; APOPTOSIS; CASE-CONTROL STUDIES; CELL SURVIVAL; CYSTIC FIBROSIS; EXTRACELLULAR TRAPS; HUMANS; INFLAMMATION; NEUTROPHILS; SWINE; TIME FACTORS;

EID: 85048178148     PISSN: 00406376     EISSN: 14683296     Source Type: Journal    
DOI: 10.1136/thoraxjnl-2017-210134     Document Type: Article

References (52)

1. Morgan WJ, ButleRSM, Johnson CA, et al. Epidemiologic study of cystic fibrosis: Design and implementation of a prospective, multicenter, observational study of patients with cystic fibrosis in the U.S., Canada. PediatRPulmonol 1999;28:231-41.
2. Bartlett JA, FischeRAJ, McCray PB. Innate immune functions of the airway epithelium. Contrib Microbiol 2008;15:147-63.
3. Jones HR, Robb CT, Perretti M, et al. The role of neutrophils in inflammation resolution. Semin Immunol 2016;28:137-45.
4. Moriceau S, LenoiRG, Witko-Sarsat V. In cystic fibrosis homozygotes and heterozygotes, neutrophil apoptosis is delayed and modulated by diamide oRroscovitine: Evidence foRan innate neutrophil disturbance. J Innate Immun 2010;2:260-6.
5. Dibbert B, WebeRM, Nikolaizik WH, et al. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: A general mechanism to accumulate effectoRcells in inflammation. Proc Natl Acad Sci USA 1999;96:13330-5.
6. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellulaRtraps kill bacteria. Science 2004;303:1532-5.
7. Brinkmann V, Zychlinsky A. Beneficial suicide: Why neutrophils die to make NETs. Nat Rev Microbiol 2007;5:577-82.
8. DwyeRM, Shan Q, D'Ortona S, et al. Cystic fibrosis sputum DNA has NETosis characteristics and neutrophil extracellulaRtrap release is regulated by macrophage migration-inhibitory factor. J Innate Immun 2014;6:765-79.
9. ManzenreiteRR, KienbergeRF, Marcos V, et al. Ultrastructural characterization of cystic fibrosis sputum using atomic force and scanning electron microscopy. J Cyst Fibros 2012;11:84-92.
10. Mitroulis I, Kambas K, Chrysanthopoulou A, et al. Neutrophil extracellulaRtrap formation is associated with IL-1and autophagy-related signaling in gout. PLoS One 2011;6:e29318.
11. KhandpuRR, Carmona-Rivera C, Vivekanandan-Giri A, et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 2013:5:178-40.
12. G arcia-Romo GS, Caielli S, Vega B, et al. Netting neutrophils are majoRinducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011:3:73-20.
13. Warnatsch A, Ioannou M, Wang Q, et al. Inflammation. Neutrophil extracellulaRtraps license macrophages foRcytokine production in atherosclerosis. Science 2015;349:316-20.
14. Zhang PX, Cheng J, Zou S, et al. Pharmacological modulation of the AKT/microRNA-199a-5p/CAV1 pathway ameliorates cystic fibrosis lung hyper-inflammation. Nat Commun 2015;6:6221.
15. Gray RD, Lucas CD, MacKellaRA, et al. Activation of conventional protein kinase C (PKC) is critical in the generation of human neutrophil extracellulaRtraps. J Inflamm 2013;10:12.
16. Lucas CD, Allen KC, Dorward DA, et al. Flavones induce neutrophil apoptosis by down-regulation of Mcl-1 via a proteasomal-dependent pathway. Faseb J 2013;27:1084-94.
17. Lucas CD, Dorward DA, Tait MA, et al. Downregulation of Mcl-1 has anti-inflammatory pro-resolution effects and enhances bacterial clearance from the lung. Mucosal Immunol 2014;7:857-68.
18. MetzleRKD, Fuchs TA, Nauseef WM, et al. Myeloperoxidase is required foRneutrophil extracellulaRtrap formation: Implications foRinnate immunity. Blood 2011;117:953-9.
19. Jeffery U, Kimura K, Gray R, et al. Dogs cast NETs too: Canine neutrophil extracellulaRtraps in health and immune-mediated hemolytic anemia. Vet Immunol Immunopathol 2015;168:262-8.
20. Ramsey BW, Davies J, McElvaney NG, et al. A CFTRpotentiatoRin patients with cystic fibrosis and the G551D mutation. N Engl J Med 2011;365:1663-72.
21. Hisert KB, Schoenfelt KQ, Cooke G, et al. Ivacaftor-Induced Proteomic Changes Suggest Monocyte Defects May Contribute to the Pathogenesis of Cystic Fibrosis. Am J RespiRCell Mol Biol 2016;54:594-7.
22. Adam RJ, Hisert KB, Dodd JD, et al. Acute administration of ivacaftoRto people with cystic fibrosis and a G551D-CFTRmutation reveals smooth muscle abnormalities. JCI Insight 2016;1:e86183.
23. Fotouhi-Ardakani N, KebiRDE, Pierre-Charles N, et al. Role foRmyeloid nucleaRdifferentiation antigen in the regulation of neutrophil apoptosis during sepsis. Am J RespiRCrit Care Med 2010;182:341-50.
24. WirnsbergeRG, Hebenstreit D, Posselt G, et al. IL-4 induces expression of TARC/CCL17 via two STAT 6 binding sites. EuRJ Immunol 2006;36:1882-91.
25. Martinez FO, Sica A, Mantovani A, et al. Macrophage activation and polarization. Front Biosci 2008;13:453-61.
26. Moriceau S, Kantari C, Mocek J, et al. Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: Potential implication in neutrophils from cystic fibrosis patients. J Immunol 2009;182:7254-63.
27. Pohl K, Hayes E, Keenan J, et al. A neutrophil intrinsic impairment affecting Rab27a and degranulation in cystic fibrosis is corrected by CFTRpotentiatoRtherapy. Blood 2014;124:999-1009.
28. BratcheRPE, Rowe SM, Reeves G, et al. Alterations in blood leukocytes of G551Dbearing cystic fibrosis patients undergoing treatment with ivacaftor. J Cyst Fibros 2016;15:67-73.
29. PainteRRG, Bonvillain RW, Valentine VG, et al. The role of chloride anion and CFTRin killing of Pseudomonas aeruginosa by normal and CF neutrophils. J Leukoc Biol 2008;83:1345-53.
30. Di A, Brown ME, Deriy LV, et al. CFTRregulates phagosome acidification in macrophages and alters bactericidal activity. Nat Cell Biol 2006;8:933-44.
31. Ng HP, Valentine VG, Wang G. CFTRtargeting during activation of human neutrophils. J Leukoc Biol 2016;100:1413-24.
32. Ng HP, Zhou Y, Song K, et al. Neutrophil-mediated phagocytic host defense defect in myeloid Cftr-inactivated mice. PLoS One 2014;9:e106813.
33. Paemka L, McCullagh BN, Abou Alaiwa MH, et al. Monocyte derived macrophages from CF pigs exhibit increased inflammatory responses at birth. J Cyst Fibros 2017;16:471-4.
34. Öz HH, Zhou B, Voss P, et al. Pseudomonas aeruginosa airway infection recruits and modulates neutrophilic Myeloid-Derived SuppressoRCells. Front Cell Infect Microbiol 2016;6:167.
35. Tirouvanziam R, Gernez Y, Conrad CK, et al. Profound functional and signaling changes in viable inflammatory neutrophils homing to cystic fibrosis airways. Proc Natl Acad Sci USA 2008;105:4335-9.
36. Makam M, Diaz D, Laval J, et al. Activation of critical, host-induced, metabolic and stress pathways marks neutrophil entry into cystic fibrosis lungs. Proc Natl Acad Sci USA 2009;106:5779-83.
37. Dorward DA, Felton JM, Robb CT, et al. The cyclin-dependent kinase inhibitoRAT 7519 accelerates neutrophil apoptosis in sepsis-related acute respiratory distress syndrome. Thorax 2017;72:182-5.
38. Young RL, Malcolm KC, Kret JE, et al. Neutrophil extracellulaRtrap (NET)-mediated killing of Pseudomonas aeruginosa: Evidence of acquired resistance within the CF airway, independent of CFTR. PLoS One 2011;6:e23637.
39. Papayannopoulos V, Staab D, Zychlinsky A. Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving DNase therapy. PLoS One 2011;6:e28526.
40. Remijsen Q, Kuijpers TW, Wirawan E, et al. Dying foRa cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death DiffeR2011;18:581-8.
41. Remijsen Q, Vanden Berghe T, Wirawan E, et al. Neutrophil extracellulaRtrap cell death requires both autophagy and superoxide generation. Cell Res 2011;21:290-304.
42. Itakura A, McCarty OJ. Pivotal role foRthe mTORpathway in the formation of neutrophil extracellulaRtraps via regulation of autophagy. Am J Physiol Cell Physiol 2013;305:C348-54.
43. Leitch AE, Lucas CD, Marwick JA, et al. Cyclin-dependent kinases 7 and 9 specifically regulate neutrophil transcription and theiRinhibition drives apoptosis to promote resolution of inflammation. Cell Death DiffeR2012;19:1950-61.
44. Wang K, Hampson P, Hazeldine J, et al. Cyclin-dependent kinase 9 activity regulates neutrophil spontaneous apoptosis. PLoS One 2012;7:e30128.
45. de la Torre AV, Junyent F, Folch J, et al. GSK3inhibition is involved in the neuroprotective effects of cyclin-dependent kinase inhibitors in neurons. Pharmacol Res 2012;65:66-73.
46. Giambelluca MS, CloutieRN, Rollet-Labelle E, et al. Expression and regulation of glycogen synthase kinase 3 in human neutrophils. Int J Biochem Cell Biol 2013;45:2660-5.
47. Scapini P, Marini O, Tecchio C, et al. Human neutrophils in the saga of cellulaRheterogeneity: Insights and open questions. Immunol Rev 2016;273:48-60.
48. Villanueva E, Yalavarthi S, BerthieRCC, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 2011;187:538-52.
49. Wright HL, Makki FA, Moots RJ, et al. Low-density granulocytes: Functionally distinct, immature neutrophils in rheumatoid arthritis with altered properties and defective TNF signalling. J Leukoc Biol 2017;101:599-611.
50. Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellulaRtraps is a silent process. J Immunol 2013;191:2647-56.
51. McKeon DJ, Condliffe AM, Cowburn AS, et al. Prolonged survival of neutrophils from patients with Delta F508 CFTRmutations. Thorax 2008;63:660-1.
52. Wainwright CE, Elborn JS, Ramsey BW, et al. Lumacaftor-IvacaftoRin Patients with Cystic Fibrosis Homozygous foRPhe508del CFTR. N Engl J Med 2015;373:220-31.