The BLT1 inhibitory function of α-1 antitrypsin augmentation therapy disrupts leukotriene B4 neutrophil signaling

Journal of Immunology

Volumn 195, Issue 8, 2015, Pages 3628-3641

  O'Dwyer, Ciara A ^a   O'Brien, M Emmet ^a   Wormald, Mark R ^b   White, Michelle M ^a   Banville, Nessa ^a   Hurley, Killian ^a   McCarthy, Cormac ^a   McElvaney, Noel G ^a   Reeves, Emer P ^a  

^a BEAUMONT HOSPITAL   (Ireland)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN CONCENTRATE; BLT1 PROTEIN; LEUKOCYTE ELASTASE; LEUKOTRIENE B4; LEUKOTRIENE RECEPTOR; UNCLASSIFIED DRUG; ALPHA 1 ANTITRYPSIN; LEUKOTRIENE B4 RECEPTOR; LTB4R PROTEIN, HUMAN;

ADULT; ALPHA 1 ANTITRYPSIN DEFICIENCY; ARTICLE; CELL ADHESION; CLINICAL ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DEGRANULATION; DRUG PROTEIN BINDING; DRUG RESPONSE; ENZYME REPLACEMENT; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MIDDLE AGED; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; ALPHA 1-ANTITRYPSIN DEFICIENCY; CALCIUM SIGNALING; IMMUNOLOGY; LUNG; NEUTROPHIL; PATHOLOGY;

ADULT; ALPHA 1-ANTITRYPSIN; ALPHA 1-ANTITRYPSIN DEFICIENCY; CALCIUM SIGNALING; CELL DEGRANULATION; FEMALE; HUMANS; LEUKOCYTE ELASTASE; LEUKOTRIENE B4; LUNG; MALE; NEUTROPHILS; RECEPTORS, LEUKOTRIENE B4;

EID: 84943526361     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500038     Document Type: Article

References (90)

1. Sadik, C. D., T. Sezin, and N. D. Kim. 2013. Leukotrienes orchestrating allergic skin inflammation. Exp. Dermatol. 22:705-709.
2. Busse, W. W. 1998. Leukotrienes and inflammation. Am. J. Respir. Crit. Care Med. 157:S210-S213.
3. 4 is a potent in vivo and in vitro eosinophil chemotactic factor in nonallergic asthma. J. Allergy Clin. Immunol. 91:634-642.
4. 4 induces degranulation. J. Allergy Clin. Immunol. 116:578-585.
5. 4, an activation product of mast cells, is a chemoattractant for their progenitors. J. Exp. Med. 201:1961-1971.
6. 4 receptor 1 expression on dendritic cells is required for the development of Th2 responses and allergen-induced airway hyperresponsiveness. J. Immunol. 181:1170-1178.
7. Hedi, H., and G. Norbert. 2004. 5-Lipoxygenase ppathway, dendritic cells, and adaptive immunity. J. Biomed. Biotechnol. 2004:99-105.
8. 4 receptor (BLT1) is required for effector CD8+ T cell-mediated, mast cell-dependent airway hyperresponsiveness. J. Immunol. 176:3157-3164.
9. Cho, N. K., Y. C. Joo, J. D. Wei, J. I. Park, and J. H. Kim. 2013. BLT2 is a protumorigenic mediator during cancer progression and a therapeutic target for anticancer drug development. Am. J. Cancer Res. 3:347-355.
10. 4 receptor BLT1 for neutrophil recruitment in inflammatory arthritis. J. Exp. Med. 203:829-835.
11. 4 in allergic diseases. Allergol. Int. 57:291-298.
12. 4-driven neutrophil recruitment to the skin is essential for allergic skin inflammation. Immunity 37:747-758.
13. 4 that mediates chemotaxis. Nature 387:620-624.
14. Massoumi, R., and A. Sjölander. 2007. The role of leukotriene receptor signaling in inflammation and cancer. ScientificWorldJournal 7:1413-1421.
15. 4 by alveolar macrophages. J. Clin. Invest. 88:891-897.
16. Iversen, L., K. Kragballe, and V. A. Ziboh. 1997. Significance of leukotriene-A4 hydrolase in the pathogenesis of psoriasis. Skin Pharmacol. 10:169-177.
17. Mackerness, K. J., G. R. Jenkins, A. Bush, and P. J. Jose. 2008. Characterisation of the range of neutrophil stimulating mediators in cystic fibrosis sputum. Thorax 63:614-620.
18. 4 antagonism in a primate model of asthma. J. Clin. Invest. 97:381-387.
19. 4 receptor subtypes (BLT1 and BLT2) in human synovial tissues and synovial fluid leukocytes of patients with rheumatoid arthritis. J. Rheumatol. 30:1712-1718.
20. Greally, P., M. J. Hussein, A. J. Cook, A. P. Sampson, P. J. Piper, and J. F. Price. 1993. Sputum tumour necrosis factor-alpha and leukotriene concentrations in cystic fibrosis. Arch. Dis. Child. 68:389-392.
21. 4 in asthmatic patients. Int. J. Tissue React. 15:181-184.
22. 4 receptor-1 is essential for allergen-mediated recruitment of CD8+ T cells and airway hyperresponsiveness. J. Immunol. 174:4979-4984.
23. 4 levels in patients with obstructive pulmonary disease. Chest 99:289-291.
24. Rask-Madsen, J., K. Bukhave, L. S. Laursen, and K. Lauritsen. 1994. 5-Lipoxygenase inhibitors in the treatment of inflammatory bowel disease. Adv. Prostaglandin Thromboxane Leukot. Res. 22:113-124.
25. 4 in murine dermatitis models. Biochem. Pharmacol. 55:297-304.
26. Singh, R. K., R. Tandon, S. G. Dastidar, and A. Ray. 2013. A review on leukotrienes and their receptors with reference to asthma. J. Asthma 50:922-931.
27. 4 receptor antagonist) for the treatment of lung disease in children and adults with cystic fibrosis. J. Cyst. Fibros. 13:148-155.
28. Bergin, D. A., E. P. Reeves, K. Hurley, R. Wolfe, R. Jameel, S. Fitzgerald, and N. G. McElvaney. 2014. The circulating proteinase inhibitor α-1 antitrypsin regulates neutrophil degranulation and autoimmunity. Sci. Transl. Med. 6:217ra1.
29. Bergin, D. A., E. P. Reeves, P. Meleady, M. Henry, O. J. McElvaney, T. P. Carroll, C. Condron, S. H. Chotirmall, M. Clynes, S. J. O'Neill, and N. G. McElvaney. 2010. α-1 Antitrypsin regulates human neutrophil chemotaxis induced by soluble immune complexes and IL-8. J. Clin. Invest. 120:4236-4250.
30. 1-Antitrypsin suppresses TNF-α and MMP-12 production by cigarette smoke-stimulated macrophages. Am. J. Respir. Cell Mol. Biol. 37:144-151.
31. 1-Antitrypsin inhalation reduces airway inflammation in cystic fibrosis patients. Eur. Respir. J. 29:240-250.
32. Kalis, M., R. Kumar, S. Janciauskiene, A. Salehi, and C. M. Cilio. 2010. a 1-Antitrypsin enhances insulin secretion and prevents cytokine-mediated apoptosis in pancreatic β-cells. Islets 2:185-189.
33. Grimstein, C., Y. K. Choi, C. H. Wasserfall, M. Satoh, M. A. Atkinson, M. L. Brantly, M. Campbell-Thompson, and S. Song. 2011. Alphα-1 antitrypsin protein and gene therapies decrease autoimmunity and delay arthritis development in mouse model. J. Transl. Med. 9:21.
34. He, S. H., H. Xie, X. J. Zhang, and X. J. Wang. 2004. Inhibition of histamine release from human mast cells by natural chymase inhibitors. Acta Pharmacol. Sin. 25:822-826.
35. 1-antitrypsin deficiency. Eur. Respir. J. 40:561-569.
36. 1-proteinase inhibitor, Zemaira. COPD 3:17-23.
37. 1-antitrypsin therapy in cystic fibrosis. Pediatr. Pulmonol. 41:177-183.
38. Wewers, M. D., M. A. Casolaro, S. E. Sellers, S. C. Swayze, K. M. McPhaul, J. T. Wittes, and R. G. Crystal. 1987. Replacement therapy for alpha1-antitrypsin deficiency associated with emphysema. N. Engl. J. Med. 316:1055-1062.
39. 1-protease inhibitor deficiency before and during therapy with IV α1-protease inhibitor. Chest 119:737-744.
40. 1-antitrypsin deficiency. Eur. Respir. J. 33:1345-1353.
41. 1 antitrypsin deficiency (RAPID): a randomised, double-blind, placebo-controlled trial. Lancet 386:360-368.
42. Russi, E. W. 2008. Alphα-1 antitrypsin: now available, but do we need it? Swiss Med. Wkly. 138:191-196.
43. 1-antitrypsin deficiency. Am. J. Respir. Crit. Care Med. 165:1494-1498.
44. Reeves, E. P., N. Banville, D. M. Ryan, N. O'Reilly, D. A. Bergin, K. Pohl, K. Molloy, O. J. McElvaney, K. Alsaleh, A. Aljorfi, et al. 2013. Intracellular secretory leukoprotease inhibitor modulates inositol 1, 4, 5-triphosphate generation and exerts an anti-inflammatory effect on neutrophils of individuals with cystic fibrosis and chronic obstructive pulmonary disease. BioMed Res. Int. 2013:560141.
45. Saeki, K., K. Saeki, M. Nakahara, S. Matsuyama, N. Nakamura, Y. Yogiashi, A. Yoneda, M. Koyanagi, Y. Kondo, and A. Yuo. 2009. A feeder-free and efficient production of functional neutrophils from human embryonic stem cells. Stem Cells 27:59-67.
46. Peres, C. M., D. M. Aronoff, C. H. Serezani, N. Flamand, L. H. Faccioli, and M. Peters-Golden. 2007. Specific leukotriene receptors couple to distinct G proteins to effect stimulation of alveolar macrophage host defense functions. J. Immunol. 179:5454-5461.
47. 4 enhances tumour necrosis factor-α-induced CCL27 production in human keratinocytes. Clin. Exp. Allergy 37:1074-1082.
48. 4 activates intracellular calcium and augments human osteoclastogenesis. Arthritis Res. Ther. 16:496.
49. Virchow, S., N. Ansorge, H. Rübben, G. Siffert, and W. Siffert. 1998. Enhanced fMLP-stimulated chemotaxis in human neutrophils from individuals carrying the G protein b3 subunit 825 T-allele. FEBS Lett. 436:155-158.
50. Jayachandran, R., V. Sundaramurthy, B. Combaluzier, P. Mueller, H. Korf, K. Huygen, T. Miyazaki, I. Albrecht, J. Massner, and J. Pieters. 2007. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell 130:37-50.
51. 4) to human serum albumin: evidence from spectroscopic, molecular modeling, and competitive displacement studies. Bioorg. Med. Chem. Lett. 15:3725-3731.
52. Gill, S. C., and P. H. von Hippel. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:319-326.
53. 1-antitrypsin stimulates the release of monocyte chemotactic protein-1 from lung epithelial cells: potential role in emphysema. Am. J. Physiol. Lung Cell. Mol. Physiol. 297:L388-L400.
54. 1-antitrypsin co-localize with neutrophils in emphysematous alveoli and are chemotactic in vivo. Am. J. Pathol. 166:377-386.
55. McCarthy, C., R. Saldova, M. R. Wormald, P. M. Rudd, N. G. McElvaney, and E. P. Reeves. 2014. The role and importance of glycosylation of acute phase proteins with focus on α-1 antitrypsin in acute and chronic inflammatory conditions. J. Proteome Res. 13:3131-3143.
56. Roversi, P., B. Ryffel, D. Togbe, I. Maillet, M. Teixeira, N. Ahmat, G. C. Paesen, O. Lissina, W. Boland, K. Ploss, et al. 2013. Bifunctional lipocalin ameliorates murine immune complex-induced acute lung injury. J. Biol. Chem. 288:18789-18802.
57. Grosdidier, A., V. Zoete, and O. Michielin. 2011. SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res. 39:W270-7.
58. Grosdidier, A., V. Zoete, and O. Michielin. 2011. Fast docking using the CHARMM force field with EADock DSS. J. Comput. Chem. 32:2149-2159.
59. Reeves, E. P., T. Ali, P. Leonard, S. Hearty, R. O'Kennedy, F. E. May, B. R. Westley, C. Josenhans, M. Rust, S. Suerbaum, et al. 2008. Helicobacter pylori lipopolysaccharide interacts with TFF1 in a pH-dependent manner. Gastroenterology 135:2043-2054, 2054.e1-2054.e2.
60. + level and action of phorbol myristate acetate. J. Clin. Invest. 79:1226-1233.
61. Korkmaz, B., S. Attucci, M. A. Juliano, T. Kalupov, M. L. Jourdan, L. Juliano, and F. Gauthier. 2008. Measuring elastase, proteinase 3 and cathepsin G activities at the surface of human neutrophils with fluorescence resonance energy transfer substrates. Nat. Protoc. 3:991-1000.
62. 4 action on endothelium mediates augmented neutrophil/endothelial adhesion. Proc. Natl. Acad. Sci. USA 81:2191-2193.
63. Naccache, P. H., H. J. Showell, E. L. Becker, and R. I. Sha'afi. 1979. Arachidonic acid induced degranulation of rabbit peritoneal neutrophils. Biochem. Biophys. Res. Commun. 87:292-299.
64. 4 is a potent chemotaxin but a weak secretagogue for human PMN. Prostaglandins 25:281-289.
65. Bokoch, G. M. 1995. Chemoattractant signaling and leukocyte activation. Blood 86:1649-1660.
66. 4 binding to recombinant BLT1. J. Mol. Biol. 329:801-814.
67. 1-antitrypsin revealed by theory and experiment. Biophys. J. 102:2856-2865.
68. Parfrey, H., R. Mahadeva, N. A. Ravenhill, A. Zhou, T. R. Dafforn, R. C. Foreman, and D. A. Lomas. 2003. Targeting a surface cavity of alpha 1-antitrypsin to prevent conformational disease. J. Biol. Chem. 278:33060-33066.
69. 4 receptor, BLT1. Int. Immunopharmacol. 3:1829-1839.
70. Ogushi, F., G. A. Fells, R. C. Hubbard, S. D. Straus, and R. G. Crystal. 1987. Ztype alpha 1-antitrypsin is less competent than M1-type alpha 1-antitrypsin as an inhibitor of neutrophil elastase. J. Clin. Invest. 80:1366-1374.
71. Bergin, D. A., K. Hurley, N. G. McElvaney, and E. P. Reeves. 2012. Alphα-1 antitrypsin: a potent anti-inflammatory and potential novel therapeutic agent. Arch. Immunol. Ther. Exp. (Warsz.) 60:81-97.
72. Bucurenci, N., D. R. Blake, K. Chidwick, and P. G. Winyard. 1992. Inhibition of neutrophil superoxide production by human plasma alpha 1-antitrypsin. FEBS Lett. 300:21-24.
73. 1-antitrypsin. Am. J. Respir. Cell Mol. Biol. 24:747-754.
74. Stockley, R. A., J. Shaw, S. C. Afford, H. M. Morrison, and D. Burnett. 1990. Effect of alphα-1-proteinase inhibitor on neutrophil chemotaxis. Am. J. Respir. Cell Mol. Biol. 2:163-170.
75. Hurley, K., N. Lacey, C. A. O'Dwyer, D. A. Bergin, O. J. McElvaney, M. E. O'Brien, O. F. McElvaney, E. P. Reeves, and N. G. McElvaney. 2014. Alphα-1 antitrypsin augmentation therapy corrects accelerated neutrophil apoptosis in deficient individuals. J. Immunol. 193:3978-3991.
76. 1-Antitrypsin regulates CD14 expression and soluble CD14 levels in human monocytes in vitro. Int. J. Biochem. Cell Biol. 39:1165-1176.
77. 1-Antitrypsin gene therapy modulates cellular immunity and efficiently prevents type 1 diabetes in nonobese diabetic mice. Hum. Gene Ther. 17:625-634.
78. 4 receptors in COPD. Chest 129:1523-1530.
79. 4 receptor BLT1 mediates early effector T cell recruitment. Nat. Immunol. 4:982-990.
80. Ford-Hutchinson, A. W., M. A. Bray, M. V. Doig, M. E. Shipley, and M. J. Smith. 1980. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature 286:264-265.
81. Birrer, P., N. G. McElvaney, A. Rüdeberg, C. W. Sommer, S. Liechti-Gallati, R. Kraemer, R. Hubbard, and R. G. Crystal. 1994. Protease-antiprotease imbalance in the lungs of children with cystic fibrosis. Am. J. Respir. Crit. Care Med. 150:207-213.
82. 1-antitrypsin therapy in elastase-induced pulmonary emphysema. Am. J. Respir. Cell Mol. Biol. 51:536-549.
83. Karnaukhova, E., S. S. Krupnikova, M. Rajabi, and A. I. Alayash. 2012. Heme binding to human alphα-1 proteinase inhibitor. Biochim. Biophys. Acta 1820:2020-2029.
84. 1-antitrypsin causes loss of anti-neutrophil elastase activity. J. Biol. Chem. 275:27258-27265.
85. 1-antitrypsin promotes aggregation. J. Mol. Biol. 396:375-383.
86. 1-antitrypsin shows variability of the reactive center and other loops. J. Mol. Biol. 306:109-119.
87. 1-antitrypsin-related emphysema. Am. J. Respir. Cell Mol. Biol. 31:133-139.
88. 1-antitrypsin deficiency. Eur. Respir. J. 43:1501-1504.
89. 4 binding to BLT1. Biochemistry 45:5733-5744.
90. Döring, G., A. Bragonzi, M. Paroni, F. F. Aktürk, C. Cigana, A. Schmidt, D. Gilpin, S. Heyder, T. Born, C. Smaczny, et al. 2014. BIIL 284 reduces neutrophil numbers but increases P. aeruginosa bacteremia and inflammation in mouse lungs. J. Cyst. Fibros. 13:156-163.