A neutrophil intrinsic impairment affecting Rab27a and degranulation in cystic fibrosis is corrected by CFTR potentiator therapy

Blood

Volumn 124, Issue 7, 2014, Pages 999-1009

  Pohl, Kerstin ^a   Hayes, Elaine ^a   Keenan, Joanne ^b   Henry, Michael ^b   Meleady, Paula ^b   Molloy, Kevin ^a   Jundi, Bakr ^a   Bergin, David A ^a   McCarthy, Cormac ^a   McElvaney, Oliver J ^a   White, Michelle M ^a   Clynes, Martin ^b   Reeves, Emer P ^a   McElvaney, Noel G ^a  

^a BEAUMONT HOSPITAL   (Ireland)

^b DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GELATINASE B; ION CHANNEL; IVACAFTOR; LACTOFERRIN; MAGNESIUM; MEMBRANE PROTEIN; MYELOPEROXIDASE; NEUTROPHIL GRANULE PROTEIN; PLASMA PROTEIN; RAB27A PROTEIN; SNARE PROTEIN; SYNAPTOBREVIN 2; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; AMINOPHENOL DERIVATIVE; CFTR PROTEIN, HUMAN; CHLORIDE; N-(2,4-DI-TERT-BUTYL-5-HYDROXYPHENYL)-4-OXO-1,4-DIHYDROQUINOLINE-3-CARBOXAMIDE; PROTEOME; QUINOLONE DERIVATIVE; RAB PROTEIN; RAB27A PROTEIN, HUMAN; SODIUM; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; CELL ACTIVATION; CELL MIGRATION; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYSTIC FIBROSIS; DEGRANULATION; DISEASE EXACERBATION; DOWN REGULATION; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE MUTATION; HETEROZYGOTE; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MAGNESIUM BLOOD LEVEL; MASS SPECTROMETER; MEMBRANE BINDING; NEUTROPHIL; NEUTROPHIL GRANULE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; TANDEM MASS SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING; X RAY MICROANALYSIS; CELL CULTURE; DRUG EFFECTS; FEMALE; GENETICS; IMMUNOBLOTTING; MALE; METABOLISM; MUTATION; PHYSIOLOGY; PROCEDURES; PROTEIN TRANSPORT; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; YOUNG ADULT;

ADULT; AMINOPHENOLS; CELL DEGRANULATION; CELLS, CULTURED; CHLORIDES; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HOMEOSTASIS; HUMANS; IMMUNOBLOTTING; MAGNESIUM; MALE; MUTATION; NEUTROPHILS; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS; QUINOLONES; RAB GTP-BINDING PROTEINS; SODIUM; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84905992903     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-02-555268     Document Type: Article

References (80)

1. Zielenski J, Tsui LC. Cystic fibrosis: genotypic and phenotypic variations. Annu Rev Genet. 1995;29:777-807. (Pubitemid 26005359)
2. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7(9):678-689. (Pubitemid 47327397)
3. Accurso FJ, Rowe SM, Clancy JP, et al. Effect of VX-770 in persons with cystic fibrosis and the G551D-CFTR mutation. N Engl J Med. 2010;363(21):1991- 2003.
4. Ramsey BW, Davies J, McElvaney NG, et al; VX08-770-102 Study Group. A CFTR potentiator in patients with cystic fibrosis and the G551D mutation. N Engl J Med. 2011;365(18):1663-1672.
5. Birrer P, McElvaney NG, Rüdeberg A, et al. Protease-antiprotease imbalance in the lungs of children with cystic fibrosis. Am J Respir Crit Care Med. 1994;150(1):207-213. (Pubitemid 24209960)
6. McElvaney NG, Nakamura H, Birrer P, et al. Modulation of airway inflammation in cystic fibrosis. In vivo suppression of interleukin-8 levels on the respiratory epithelial surface by aerosolization of recombinant secretory leukoprotease inhibitor. J Clin Invest. 1992;90(4):1296-1301.
7. Painter RG, Valentine VG, Lanson NA Jr, et al. CFTR expression in human neutrophils and the phagolysosomal chlorination defect in cystic fibrosis. Biochemistry. 2006;45(34):10260-10269. (Pubitemid 44384801)
8. Zhou Y, Song K, Painter RG, et al. Cystic fibrosis transmembrane conductance regulator recruitment to phagosomes in neutrophils. J Innate Immun. 2013;5(3):219-230.
9. Hayes E, Pohl K, McElvaney NG, Reeves EP. The cystic fibrosis neutrophil: a specialized yet potentially defective cell. Arch Immunol Ther Exp (Warsz). 2011;59(2):97-112.
10. Alexis NE, Muhlebach MS, Peden DB, Noah TL. Attenuation of host defense function of lung phagocytes in young cystic fibrosis patients. J Cyst Fibros. 2006;5(1):17-25. (Pubitemid 43137157)
11. Moraes TJ, Plumb J, Martin R, et al. Abnormalities in the pulmonary innate immune system in cystic fibrosis. Am J Respir Cell Mol Biol. 2006;34(3):364-374. (Pubitemid 43320718)
12. Koller DY, Urbanek R, Götz M. Increased degranulation of eosinophil and neutrophil granulocytes in cystic fibrosis. Am J Respir Crit Care Med. 1995;152(2):629-633.
13. Taggart C, Coakley RJ, Greally P, Canny G, O'Neill SJ, McElvaney NG. Increased elastase release by CF neutrophils is mediated by tumor necrosis factor-alpha and interleukin-8. Am J Physiol Lung Cell Mol Physiol. 2000;278(1):L33-L41. (Pubitemid 30104172)
14. Brennan S, Cooper D, Sly PD. Directed neutrophil migration to IL-8 is increased in cystic fibrosis: a study of the effect of erythromycin. Thorax. 2001;56(1):62-64. (Pubitemid 32041721)
15. Davis PB, Drumm M, Konstan MW. Cystic fibrosis. Am J Respir Crit Care Med. 1996;154(5):1229-1256. (Pubitemid 26391164)
16. Corvol H, Fitting C, Chadelat K, et al. Distinct cytokine production by lung and blood neutrophils from children with cystic fibrosis. Am J Physiol Lung Cell Mol Physiol. 2003;284(6):L997-L1003. (Pubitemid 36687135)
17. Witko-Sarsat V, Allen RC, Paulais M, et al. Disturbed myeloperoxidase-dependent activity of neutrophils in cystic fibrosis homozygotes and heterozygotes, and its correction by amiloride. J Immunol. 1996;157(6):2728-2735. (Pubitemid 126450492)
18. Witko-Sarsat V, Delacourt C, Rabier D, Bardet J, Nguyen AT, Descamps-Latscha B. Neutrophil-derived long-lived oxidants in cystic fibrosis sputum. Am J Respir Crit Care Med. 1995;152(6 Pt 1):1910-1916.
19. Armstrong DS, Hook SM, Jamsen KM, et al. Lower airway inflammation in infants with cystic fibrosis detected by newborn screening. Pediatr Pulmonol. 2005;40(6):500-510. (Pubitemid 41720706)
20. Rosenfeld M, Gibson RL, McNamara S, et al. Early pulmonary infection, inflammation, and clinical outcomes in infants with cystic fibrosis. Pediatr Pulmonol. 2001;32(5):356-366. (Pubitemid 33015652)
21. Moriceau S, Lenoir G, Witko-Sarsat V. In cystic fibrosis homozygotes and heterozygotes, neutrophil apoptosis is delayed and modulated by diamide or roscovitine: evidence for an innate neutrophil disturbance. J Innate Immun. 2010;2(3):260-266.
22. 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(11):7254-7263.
23. Bonvillain RW, Painter RG, Adams DE, Viswanathan A, Lanson NA Jr, Wang G. RNA interference against CFTR affects HL60-derived neutrophil microbicidal function. Free Radic Biol Med. 2010;49(12):1872-1880.
24. Painter RG, Bonvillain RW, Valentine VG, et al. The role of chloride anion and CFTR in killing of Pseudomonas aeruginosa by normal and CF neutrophils. J Leukoc Biol. 2008;83(6):1345-1353. (Pubitemid 351960313)
25. Painter RG, Marrero L, Lombard GA, Valentine VG, Nauseef WM, Wang G. CFTR-mediated halide transport in phagosomes of human neutrophils. J Leukoc Biol. 2010;87(5):933-942.
26. Reeves EP, Williamson M, O'Neill SJ, Greally P, McElvaney NG. Nebulised hypertonic saline decreases interleukin-8 in sputum of patients with cystic fibrosis. Am J Respir Crit Care Med. 2011;183(11):1517-1523.
27. Reeves EP, Lu H, Jacobs HL, et al. Killing activity of neutrophils is mediated through activation of proteases by K + flux. Nature. 2002;416(6878):291-297. (Pubitemid 34260237)
28. Bergin DA, Reeves EP, Hurley K, et al. The circulating proteinase inhibitor alpha-1 antitrypsin regulates neutrophil degranulation and autoimmunity. Sci Transl Med. 2014;6(217):217ra211.
29. Saeki K, Saeki K, Nakahara M, et al. A feeder-free and efficient production of functional neutrophils from human embryonic stem cells. Stem Cells. 2009;27(1):59-67.
30. Meshkini A, Yazdanparast R, Nouri K. Intracellular GTP level determines cell's fate toward differentiation and apoptosis. Toxicol Appl Pharmacol. 2011;253(3):188-196.
31. Bergsson G, Reeves EP, McNally P, et al. LL-37 complexation with glycosaminoglycans in cystic fibrosis lungs inhibits antimicrobial activity, which can be restored by hypertonic saline. J Immunol. 2009;183(1):543-551.
32. Bergin DA, Reeves EP, Meleady P, et al. α-1 Antitrypsin regulates human neutrophil chemotaxis induced by soluble immune complexes and IL-8. J Clin Invest. 2010;120(12):4236-4250.
33. Scheele JS, Rhee JM, Boss GR. Determination of absolute amounts of GDP and GTP bound to Ras in mammalian cells: comparison of parental and Ras-overproducing NIH 3T3 fibroblasts. Proc Natl Acad Sci USA. 1995;92(4):1097-1100.
34. McLaughlin CW, Peart D, Purves RD, Carré DA, Macknight AD, Civan MM. Effects of HCO3- on cell composition of rabbit ciliary epithelium: a new model for aqueous humor secretion. Invest Ophthalmol Vis Sci. 1998;39(9):1631-1641. (Pubitemid 28361323)
35. Simchowitz L, De Weer P. Chloride movements in human neutrophils. Diffusion, exchange, and active transport. J Gen Physiol. 1986;88(2):167-194. (Pubitemid 16041656)
36. Lodish HBA, Zipursky SL, Matsudaira P, Baltimore D. Molecular Cell Biology, 4th Ed. W.H. Freeman, New York; 2000.
37. Caci E, Caputo A, Hinzpeter A, et al. Evidence for direct CFTR inhibition by CFTR(inh)-172 based on Arg347 mutagenesis. Biochem J. 2008;413(1):135-142. (Pubitemid 351946869)
38. Ma T, Thiagarajah JR, Yang H, et al. Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest. 2002;110(11):1651-1658. (Pubitemid 35424243)
39. Pilas B, Durack G. A flow cytometric method for measurement of intracellular chloride concentration in lymphocytes using the halide-specific probe 6-methoxy-N-(3-sulfopropyl) quinolinium (SPQ). Cytometry. 1997;28(4):316-322. (Pubitemid 27359608)
40. Tashiro M, Konishi M. Basal intracellular free Mg2+ concentration in smooth muscle cells of guinea pig tenia cecum: intracellular calibration of the fluorescent indicator furaptra. Biophys J. 1997;73(6):3358-3370. (Pubitemid 27525798)
41. Janusonis S. Comparing two small samples with an unstable, treatment-independent baseline. J Neurosci Methods. 2009;179(2):173-178.
42. Kronborg G, Hansen MB, Svenson M, Fomsgaard A, Høiby N, Bendtzen K. Cytokines in sputum and serum from patients with cystic fibrosis and chronic Pseudomonas aeruginosa infection as markers of destructive inflammation in the lungs. Pediatr Pulmonol. 1993;15(5):292-297.
43. Richter J, Ng-Sikorski J, Olsson I, Andersson T. Tumor necrosis factor-induced degranulation in adherent human neutrophils is dependent on CD11b/CD18-integrin-triggered oscillations of cytosolic free Ca2+. Proc Natl Acad Sci USA. 1990;87(23):9472-9476. (Pubitemid 120030649)
44. Niessen HW, Verhoeven AJ. Differential up-regulation of specific and azurophilic granule membrane markers in electropermeabilized neutrophils. Cell Signal. 1992;4(5):501-509.
45. Herrero-Turrión MJ, Calafat J, Janssen H, Fukuda M, Mollinedo F. Rab27a regulates exocytosis of tertiary and specific granules in human neutrophils. J Immunol. 2008;181(6):3793-3803.
46. Neeft M, Wieffer M, de Jong AS, et al. Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. Mol Biol Cell. 2005;16(2):731-741. (Pubitemid 40173984)
47. Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007;28(8):340-345. (Pubitemid 47077924)
48. Mollinedo F, Martín-Martín B, Calafat J, Nabokina SM, Lazo PA. Role of vesicle-associated membrane protein-2, through Q-soluble N-ethylmaleimide-sensitive factor attachment protein receptor/R-soluble N-ethylmaleimide-sensitive factor attachment protein receptor interaction, in the exocytosis of specific and tertiary granules of human neutrophils. J Immunol. 2003;170(2):1034-1042. (Pubitemid 36070559)
49. Stow JL, Manderson AP, Murray RZ. SNAREing immunity: the role of SNAREs in the immune system. Nat Rev Immunol. 2006;6(12):919-929. (Pubitemid 44851734)
50. Seabra MC, Wasmeier C. Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol. 2004;16(4):451-457. (Pubitemid 38903152)
51. Sprang SR, Coleman DE. Invasion of the nucleotide snatchers: structural insights into the mechanism of G protein GEFs. Cell. 1998;95(2):155-158. (Pubitemid 28473776)
52. Gupta A, Eastham KM, Wrightson N, Spencer DA. Hypomagnesaemia in cystic fibrosis patients referred for lung transplant assessment. J Cyst Fibros. 2007;6(5):360-362. (Pubitemid 47324154)
53. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol. 2006;6(7):541-550. (Pubitemid 43980526)
54. Sørensen OE, Follin P, Johnsen AH, et al. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood. 2001;97(12):3951-3959.
55. Burns JL, Emerson J, Stapp JR, et al. Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin Infect Dis. 1998;27(1):158-163. (Pubitemid 28334435)
56. Bonfield TL, Hodges CA, Cotton CU, Drumm ML. Absence of the cystic fibrosis transmembrane regulator (Cftr) from myeloid-derived cells slows resolution of inflammation and infection. J Leukoc Biol. 2012;92(5):1111-1122.
57. Yoshimura K, Nakamura H, Trapnell BC, et al. Expression of the cystic fibrosis transmembrane conductance regulator gene in cells of non-epithelial origin. Nucleic Acids Res. 1991;19(19):5417-5423. (Pubitemid 21912942)
58. Kälin N, Claass A, Sommer M, Puchelle E, Tümmler B. DeltaF508 CFTR protein expression in tissues from patients with cystic fibrosis. J Clin Invest. 1999;103(10):1379-1389. (Pubitemid 29535494)
59. Owen CA, Hu Z, Barrick B, Shapiro SD. Inducible expression of tissue inhibitor of metalloproteinases-resistant matrix metalloproteinase-9 on the cell surface of neutrophils. Am J Respir Cell Mol Biol. 2003;29(3 Pt 1):283-294. (Pubitemid 37093986)
60. Lau D, Mollnau H, Eiserich JP, et al. Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proc Natl Acad Sci USA. 2005;102(2):431-436. (Pubitemid 40116784)
61. Perez A, Issler AC, Cotton CU, Kelley TJ, Verkman AS, Davis PB. CFTR inhibition mimics the cystic fibrosis inflammatory profile. Am J Physiol Lung Cell Mol Physiol. 2007;292(2):L383-L395.
62. Kamiya H, Ehara T, Matsumoto T. Inhibitory effects of lactoferrin on biofilm formation in clinical isolates of Pseudomonas aeruginosa. J Infect Chemother. 2012;18(1):47-52.
63. Böttcher T, Spreer A, Azeh I, Nau R, Gerber J. Matrix metalloproteinase-9 deficiency impairs host defense mechanisms against Streptococcus pneumoniae in a mouse model of bacterial meningitis. Neurosci Lett. 2003;338(3):201-204. (Pubitemid 36173748)
64. Renckens R, Roelofs JJ, Florquin S, et al. Matrix metalloproteinase-9 deficiency impairs host defense against abdominal sepsis. J Immunol. 2006;176(6):3735-3741. (Pubitemid 43364020)
65. Kuroda TS, Fukuda M, Ariga H, Mikoshiba K. The Slp homology domain of synaptotagmin-like proteins 1-4 and Slac2 functions as a novel Rab27A binding domain. J Biol Chem. 2002; 277(11):9212-9218. (Pubitemid 34953001)
66. Novak EK, Gautam R, Reddington M, et al. The regulation of platelet-dense granules by Rab27a in the ashen mouse, a model of Hermansky-Pudlak and Griscelli syndromes, is granule-specific and dependent on genetic background. Blood. 2002;100(1):128-135. (Pubitemid 35177437)
67. Ménasché G, Pastural E, Feldmann J, et al. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat Genet. 2000;25(2):173-176. (Pubitemid 30394987)
68. Abdel-Latif D, Steward M, Macdonald DL, Francis GA, Dinauer MC, Lacy P. Rac2 is critical for neutrophil primary granule exocytosis. Blood. 2004;104(3):832-839. (Pubitemid 38970582)
69. Munafó DB, Johnson JL, Ellis BA, Rutschmann S, Beutler B, Catz SD. Rab27a is a key component of the secretory machinery of azurophilic granules in granulocytes. Biochem J. 2007;402(2):229-239. (Pubitemid 46383420)
70. Brzezinska AA, Johnson JL, Munafo DB, et al. The Rab27a effectors JFC1/Slp1 and Munc13-4 regulate exocytosis of neutrophil granules. Traffic. 2008;9(12):2151-2164.
71. Johnson JL, Brzezinska AA, Tolmachova T, et al. Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic. 2010;11(4):533-547.
72. Catz SD. Regulation of vesicular trafficking and leukocyte function by Rab27 GTPases and their effectors. J Leukoc Biol. 2013;94(4):613-622.
73. Lazrak A, Jurkuvenaite A, Chen L, et al. Enhancement of alveolar epithelial sodium channel activity with decreased cystic fibrosis transmembrane conductance regulator expression in mouse lung. Am J Physiol Lung Cell Mol Physiol. 2011;301(4):L557-L567.
74. Ando-Akatsuka Y, Abdullaev IF, Lee EL, Okada Y, Sabirov RZ. Down-regulation of volume-sensitive Cl- channels by CFTR is mediated by the second nucleotide-binding domain. Pflugers Arch. 2002;445(2):177-186. (Pubitemid 35447512)
75. Yoo D, Flagg TP, Olsen O, Raghuram V, Foskett JK, Welling PA. Assembly and trafficking of a multiprotein ROMK (Kir 1.1) channel complex by PDZ interactions. J Biol Chem. 2004;279(8):6863-6873. (Pubitemid 38248829)
76. Berdiev BK, Qadri YJ, Benos DJ. Assessment of the CFTR and ENaC association. Mol Biosyst. 2009;5(2):123-127.
77. Oglesby IK, Chotirmall SH, McElvaney NG, Greene CM. Regulation of cystic fibrosis transmembrane conductance regulator by microRNA-145, -223, and -494 is altered in ΔF508 cystic fibrosis airway epithelium. J Immunol. 2013; 190(7):3354-3362.
78. Mall M, Bleich M, Greger R, Schreiber R, Kunzelmann K. The amiloride-inhibitable Na+ conductance is reduced by the cystic fibrosis transmembrane conductance regulator in normal but not in cystic fibrosis airways. J Clin Invest. 1998;102(1):15-21. (Pubitemid 28323825)
79. Vormann J, Magdorf K, Günther T, Wahn U. Increased Na+/Mg2+ antiport in erythrocytes of patients with cystic fibrosis. Eur J Clin Chem Clin Biochem. 1994;32(11):833-836. (Pubitemid 24359477)
80. Van Goor F, Hadida S, Grootenhuis PD, et al. Rescue of CF airway epithelial cell function in vitro by a CFTR potentiator, VX-770. Proc Natl Acad Sci USA. 2009;106(44):18825-18830.