CFTR inhibition provokes an inflammatory response associated with an imbalance of the annexin A1 pathway

American Journal of Pathology

Volumn 177, Issue 1, 2010, Pages 176-186

  Dalli, Jesmond ^a   Rosignoli, Guglielmo ^a   Hayhoe, Richard P G ^a   Edelman, Aleksander ^b   Perretti, Mauro ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOCORTIN 1; TRANSMEMBRANE CONDUCTANCE REGULATOR; ZYMOSAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INFLAMMATORY DISEASE; LEUKOCYTE MICROPARTICLE; LEUKOCYTE MIGRATION; MOUSE; NEUTROPHIL; NONHUMAN; PERITONEUM CELL; PERITONITIS; PHENOTYPE; PRIORITY JOURNAL;

EID: 77954613183     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091149     Document Type: Article

References (59)

1. Quinton PM: Physiological basis of cystic fibrosis: a historical perspective. Physiol Rev 1999, 79:S3-S22 (Pubitemid 29058907)
2. Balough K, McCubbin M, Weinberger M, Smits W, Ahrens R, Fick R: The relationship between infection and inflammation in the early stages of lung disease from cystic fibrosis. Pediatr Pulmonol 1995, 20:63-70
3. Bonfield TL, Panuska JR, Konstan MW, Hilliard KA, Hilliard JB, Ghnaim H, Berger M: Inflammatory cytokines in cystic fibrosis lungs. Am J Respir Crit Care Med 1995, 152:2111-2118
4. Corvol H, Fitting C, Chadelat K, Jacquot J, Tabary O, Boule M, Cavaillon JM, Clement A: Distinct cytokine production by lung and blood neutrophils from children with cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 2003, 284:L997-L1003 (Pubitemid 36687135)
5. Griese M, Kappler M, Gaggar A, Hartl D: Inhibition of airway proteases in cystic fibrosis lung disease. Eur Respir J 2008, 32:783-795
6. Khan TZ, Wagener JS, Bost T, Martinez J, Accurso FJ, Riches DW: Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med 1995, 151:1075-1082
7. Serhan CN, Brain SD, Buckley CD, Gilroy DW, Haslett C, O'Neill LA, Perretti M, Rossi AG, Wallace JL: Resolution of inflammation: state of the art, definitions and terms. FASEB J 2007, 21:325-332 (Pubitemid 46213480)
8. Serhan CN, Savill J: Resolution of inflammation: the beginning programs the end. Nat Immunol 2005, 6:1191-1197
9. Gilroy DW, Lawrence T, Perretti M, Rossi AG: Inflammatory resolution: new opportunities for drug discovery. Nat Rev Drug Discov 2004, 3:401-416 (Pubitemid 38618123)
10. Perretti M, D'Acquisto F: Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol 2009, 9:62-70
11. Perretti M, Chiang N, La M, Fierro IM, Marullo S, Getting SJ, Solito E, Serhan CN: Endogenous lipid- and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nat Med 2002, 8:1296-1302
12. Kamal AM, Flower RJ, Perretti M: An overview of the effects of annexin 1 on cells involved in the inflammatory process. Mem Inst Oswaldo Cruz 2005, 100 Suppl 1:39-47
13. Hayhoe RP, Kamal AM, Solito E, Flower RJ, Cooper D, Perretti M: Annexin 1 and its bioactive peptide inhibit neutrophil-endothelium interactions under flow: indication of distinct receptor involvement. Blood 2006, 107:2123-2130 (Pubitemid 43289398)
14. Vong L, D'Acquisto F, Pederzoli-Ribeil M, Lavagno L, Flower RJ, Witko-Sarsat V, Perretti M: Annexin 1 cleavage in activated neutrophils: a pivotal role for proteinase 3. J Biol Chem 2007, 282:29998-30004 (Pubitemid 350035249)
15. Solito E, Kamal A, Russo-Marie F, Buckingham JC, Marullo S, Perretti M: A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB J 2003, 17:1544-1546
16. Maderna P, Yona S, Perretti M, Godson C: Modulation of phagocytosis of apoptotic neutrophils by supernatant from dexamethasone-treated macrophages and annexin-derived peptide Ac(2-26). J Immunol 2005, 174:3727-3733 (Pubitemid 40354084)
17. Ferlazzo V, D'Agostino P, Milano S, Caruso R, Feo S, Cillari E, Parente L: Anti-inflammatory effects of annexin-1: stimulation of IL-10 release and inhibition of nitric oxide synthesis. Int Immunopharmacol 2003, 3:1363-1369 (Pubitemid 37025717)
18. Bensalem N, Ventura AP, Vallee B, Lipecka J, Tondelier D, Davezac N, Dos Santos A, Perretti M, Fajac A, Sermet-Gaudelus I, Renouil M, Lesure JF, Halgand F, Laprevote O, Edelman A: Down-regulation of the anti-inflammatory protein annexin A1 in cystic fibrosis knock-out mice and patients. Mol Cell Proteomics 2005, 4:1591-1601 (Pubitemid 41555482)
19. Borot F, Vieu DL, Faure G, Fritsch J, Colas J, Moriceau S, Baudouin-Legros M, Brouillard F, Ayala-Sanmartin J, Touqui L, Chanson M, Edelman A, Ollero M: Eicosanoid release is increased by membrane destabilization and CFTR inhibition in Calu-3 cells. PLoS One 2009, 4:e7116
20. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, Galietta LJ, Verkman AS: Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 2002, 110:1651-1658 (Pubitemid 35424243)
21. Hannon R, Croxtall JD, Getting SJ, Roviezzo F, Yona S, Paul-Clark MJ, Gavins FN, Perretti M, Morris JF, Buckingham JC, Flower RJ: Aberrant inflammation and resistance to glucocorticoids in annexin 1-/- mouse. FASEB J 2003, 17:253-255
22. Snouwaert JN, Brigman KK, Latour AM, Malouf NN, Boucher RC, Smithies O, Koller BH: An animal model for cystic fibrosis made by gene targeting. Science 1992, 257:1083-1088
23. Chatterjee BE, Yona S, Rosignoli G, Young RE, Nourshargh S, Flower RJ, Perretti M: Annexin 1-deficient neutrophils exhibit enhanced transmigration in vivo and increased responsiveness in vitro. J Leukoc Biol 2005, 78:639-646 (Pubitemid 41292086)
24. Muanprasat C, Sonawane ND, Salinas D, Taddei A, Galietta LJ, Verkman AS: Discovery of glycine hydrazide pore-occluding CFTR inhibitors: mechanism, structure-activity analysis, and in vivo efficacy. J Gen Physiol 2004, 124:125-137 (Pubitemid 39038187)
25. Perretti M, Croxtall JD, Wheller SK, Goulding NJ, Hannon R, Flower RJ: Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat Med 1996, 2:1259-1262 (Pubitemid 26375414)
26. Dalli J, Norling LV, Renshaw D, Cooper D, Leung KY, Perretti M: Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 2008, 112:2512-2519
27. Pepinsky RB, Sinclair LK, Dougas I, Liang CM, Lawton P, Browning JL: Monoclonal antibodies to lipocortin-1 as probes for biological function. FEBS Lett 1990, 261:247-252 (Pubitemid 20074966)
28. Collins TJ: ImageJ for microscopy. Biotechniques 2007, 43:25-30
29. Ye RD, Boulay F, Wang JM, Dahlgren C, Gerard C, Parmentier M, Serhan CN, Murphy PM: International Union of Basic and Clinical Pharmacology. LXXIII Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol Rev 2009, 61:119-161
30. Elston C, Geddes D: Inflammation in cystic fibrosis-when and why? Friend or foe? Semin Respir Crit Care Med 2007, 28:286-294
31. Fayon M: CF-Emerging therapies: Modulation inflammation. Paediatr Respir Rev 2006, 7 Suppl 1:S170-S174
32. Sharma S, Jaffe A, Dixon G: Immunomodulatory effects of macrolide antibiotics in respiratory disease: therapeutic implications for asthma and cystic fibrosis. Paediatr Drugs 2007, 9:107-118 (Pubitemid 46624563)
33. Ambrose MP, Hunninghake GW: Corticosteroids increase lipocortin I in alveolar epithelial cells. Am J Respir Cell Mol Biol 1990, 3:349-353
34. Zouki C, Ouellet S, Filep JG: The anti-inflammatory peptides, antiflammins, regulate the expression of adhesion molecules on human leukocytes and prevent neutrophil adhesion to endothelial cells. FASEB J 2000, 14:572-580 (Pubitemid 30143177)
35. Lim LH, Solito E, Russo-Marie F, Flower RJ, Perretti M: Promoting detachment of neutrophils adherent to murine postcapillary venules to control inflammation: effect of lipocortin 1. Proc Natl Acad Sci USA 1998, 95:14535-14539
36. Souza DG, Fagundes CT, Amaral FA, Cisalpino D, Sousa LP, Vieira AT, Pinho V, Nicoli JR, Vieira LQ, Fierro IM, Teixeira MM: The required role of endogenously produced lipoxin A4 and annexin-1 for the production of IL-10 and inflammatory hyporesponsiveness in mice. J Immunol 2007, 179:8533-8543
37. Scannell M, Flanagan MB, deStefani A, Wynne KJ, Cagney G, Godson C, Maderna P: Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J Immunol 2007, 178:4595-4605
38. Witko-Sarsat V, Allen RC, Paulais M, Nguyen AT, Bessou G, Lenoir G, Descamps-Latscha B: Disturbed myeloperoxidase-dependent activity of neutrophils in cystic fibrosis homozygotes and heterozygotes, and its correction by amiloride. J Immunol 1996, 157:2728-2735
39. Witko-Sarsat V, Sermet-Gaudelus I, Lenoir G, Descamps-Latscha B: Inflammation and CFTR: might neutrophils be the key in cystic fibrosis? Mediators Inflamm 1999, 8:7-11
40. Moriceau S, Kantari C, Mocek J, Davezac N, Gabillet J, Guerrera IC, Brouillard F, Tondelier D, Sermet-Gaudelus I, Danel C, Lenoir G, Daniel S, Edelman A, Witko-Sarsat V: Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: potential implication in neutrophils from cystic fibrosis patients. J Immunol 2009, 182:7254-7263
41. Watt AP, Courtney J, Moore J, Ennis M, Elborn JS: Neutrophil cell death, activation and bacterial infection in cystic fibrosis. Thorax 2005, 60:659-664
42. Bonfield TL, Konstan MW, Burfeind P, Panuska JR, Hilliard JB, Berger M: Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. Am J Respir Cell Mol Biol 1995, 13:257-261
43. Soltys J, Bonfield T, Chmiel J, Berger M: Functional IL-10 deficiency in the lung of cystic fibrosis (cftr-/-) and IL-10 knockout mice causes increased expression and function of B7 costimulatory molecules on alveolar macrophages. J Immunol 2002, 168:1903-1910
44. Kelly M, Trudel S, Brouillard F, Bouillaud F, Colas J, Nguyen-Khoa T, Ollero M, Edelman A, Fritsch J: CFTR inhibitors, CFTRinh-172 and GlyH-101 target mitochondrial functions, independently of chloride channel inhibition. J Pharmacol Exp Ther 2010, 333:60-69
45. Romano M, Collura M, Lapichino L, Pardo F, Falco A, Chiesa PL, Caimi G, Davi G: Endothelial perturbation in cystic fibrosis. Thromb Haemost 2001, 86:1363-1367
46. Perretti M, Dalli J: Exploiting the Annexin A1 pathway for the development of novel anti-inflammatory therapeutics. Br J Pharmacol 2009, 158:936-946
47. Retsch-Bogart GZ: Update on new pulmonary therapies. Curr Opin Pulm Med 2009, 15(6):604-610
48. Bartling TR, Drumm ML: Loss of CFTR results in reduction of histone deacetylase 2 in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2009, 297:L35-L43
49. Quattrucci S, Napolitano M, Valentini SB, Giuliani A, Bravo E: Neutrophil generation of inflammatory precursors is not modulated by docosahexaenoic acid. Inflamm Res 2009, 58:677-685
50. Rosales JL, Ernst JD: Calcium-dependent neutrophil secretion: characterization and regulation by annexins. J Immunol 1997, 159:6195-6202
51. Perretti M, Christian H, Wheller SK, Aiello I, Mugridge KG, Morris JF, Flower RJ, Goulding NJ: Annexin I is stored within gelatinase granules of human neutrophil and mobilized on the cell surface upon adhesion but not phagocytosis. Cell Biol Int 2000, 24:163-174
52. Lominadze G, Powell DW, Luerman GC, Link AJ, Ward RA, McLeish KR: Proteomic analysis of human neutrophil granules. Mol Cell Proteomics 2005, 4:1503-1521
53. Gavins FN, Kamal AM, D'Amico M, Oliani SM, Perretti M: Formyl-peptide receptor is not involved in the protection afforded by annexin 1 in murine acute myocardial infarct. FASEB J 2005, 19:100-102
54. Downey DG, Bell SC, Elborn JS: Neutrophils in cystic fibrosis. Thorax 2009, 64:81-88
55. Di A, Brown ME, Deriy LV, Li C, Szeto FL, Chen Y, Huang P, Tong J, Naren AP, Bindokas V, Palfrey HC, Nelson DJ: CFTR regulates phagosome acidification in macrophages and alters bactericidal activity. Nat Cell Biol 2006, 8:933-944
56. Morris MR, Doull IJ, Dewitt S, Hallett MB: Reduced iC3b-mediated phagocytotic capacity of pulmonary neutrophils in cystic fibrosis. Clin Exp Immunol 2005, 142:68-75 (Pubitemid 41361007)
57. Painter RG, Valentine VG, Lanson NA Jr, Leidal K, Zhang Q, Lombard G, Thompson C, Viswanathan A, Nauseef WM, Wang G: CFTR Expression in human neutrophils and the phagolysosomal chlorination defect in cystic fibrosis. Biochemistry 2006, 45:10260-10269 (Pubitemid 44384801)
58. Painter RG, Bonvillain RW, Valentine VG, Lombard GA, LaPlace SG, Nauseef WM, Wang G: The role of chloride anion and CFTR in killing of pseudomonas aeruginosa by normal and CF neutrophils. J Leukoc Biol 2008, 83:1345-1353
59. Koller B, Bals R, Roos D, Korting HC, Griese M, Hartl D: Innate immune receptors on neutrophils and their role in chronic lung disease. Eur J Clin Invest 2009, 39:535-547