Neutrophils and emerging targets for treatment in chronic obstructive pulmonary disease

Expert Review of Clinical Immunology

Volumn 9, Issue 11, 2013, Pages 1055-1068

  Meijer, Mariska ^a   Rijkers, Ger T ^a   Van Overveld, Frans J ^a  

^a University College Roosevelt   (Netherlands)

Author keywords

chronic obstructive pulmonary disease control; infectious agents; infiltration; inflammation; neutrophil; oxidative stress; protease imbalance; treatment

Indexed keywords

AZITHROMYCIN; BRONCHODILATING AGENT; CATHELICIDIN; CORTICOSTEROID DERIVATIVE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 8; LEUKOCYTE ELASTASE; MITOGEN ACTIVATED PROTEIN KINASE; P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN; REACTIVE OXYGEN METABOLITE; ROFLUMILAST; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

AIRFLOW; ANTIMICROBIAL ACTIVITY; ASTHMA; CHRONIC OBSTRUCTIVE LUNG DISEASE; HUMAN; LUNG INFILTRATE; LUNG INJURY; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL COUNT; OXIDATIVE STRESS; PHAGOCYTOSIS; PHAGOSOME; REVIEW; UNSPECIFIED SIDE EFFECT;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; CELL DEGRANULATION; CYTOPLASMIC GRANULES; ENZYME INHIBITORS; HUMANS; LUNG; MOLECULAR TARGETED THERAPY; NEUTROPHILS; OXIDATIVE STRESS; PHAGOCYTOSIS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE;

EID: 84887309566     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2013.851347     Document Type: Review

References (130)

1. Borregaard N. Neutrophils, from marrow to microbes. Immunity 30(5), 657-670 (2010).
2. Soenlein O. An elegant defence: how neutrophils shape the immune response. Trends Immunol. 30(11), 511-512 (2009).
3. Meijer M, Pruchniak MP, Arazna M, Demkow U. Extracellular traps: how to isolate and quantify extracellular DNA (ETDNA). Centr. Eur. J. Immunol. 37(4), 321-325 (2012).
4. Kindt TJ, Soenlein O, Osborne BA. In: Kuby Immunology (6th Edition). W.H. Freeman and Company, NY, USA (2007).
5. Hogg JC, Chu F, Utokaparch S et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N. Engl. J. Med. 350(26), 2645-2653 (2004).
6. Bruehl RE, Moore KL, Borregaard N, Zimmerman GA, McEver RP, Bainton DF. Leukocyte activation induces surface redistribution of P-selectin glycoprotein ligand-1. J. Leukoc. Biol. 61(4), 489-499 (1997).
7. Buscher K, Riese SB, Shakibaei M et al. The transmembrane domains of L-selectin and DC44 regulate cell surface positioning and leukocyte adhesion under flow. J. Biol. Chem. 285(18), 13490-13497 (2010).
8. Hidalgo A, Peired AJ, Wild MK, Vestweber D, Frenette PS. Complete identification of E-selectin ligands on neutrophils reveals distinct functions of PSGL-1, ESL-1 and CD44. Immunity 26(4), 477-489 (2007).
9. Hossain M, Qadri SM, Liu L. Inhibition of nitric oxide synthesis enhances leukocyte rolling and adhesion in human microvasculature. J. Inflamm. 9(1), 28-35 (2012).
10. Campbell JJ, Hedrick J, Zlotnik A, Siani MA, Thompson DA, Butcher EC. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279(5349), 381-384 (1998).
11. Campbell JJ, Qun SK, Bacon KB, MacKay CR, Butcher EC. Biology of chemokine and classical chemoattractant receptors. Differential requirements for adhesion-triggering versus chemotactic responses in lymphoid cells. J. Cell Biol. 134(1), 255-266 (1996).
12. Middleton J, Neil S, Wintle J et al. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91(3), 385-395 (1997).
13. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7(9), 678-689 (2007).
14. Bazzoni G, Ma L, Blue ML, Hemler ME. Divalent cations and ligands induce conformational changes that are highly divergent among beta 1 integrins. J. Biol. Chem. 273(12), 6670-6678 (2011).
15. Liu Q, Mirc D, Fu BM. Mechanical mechanisms of thrombosis in intact bent microvessels of rat mesentery. J. Biomech. 41(12), 2726-2734 (2008).
16. Sengupta K, Aranda-Espinoza H, Smith L, Janmey P, Hammer D. Spreading of neutrophils: from activation to migration. Biophys. J. 91(12), 4638-4648 (2006).
17. Phillipson M, Heit B, Colarusso P, Liu L, Ballantyne CM, Kubes P. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 203(12), 2569-2575 (2006).
18. Schenkel AR, Mamdouh Z, Muller WA. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat. Immunol. 5(4), 393-400 (2012).
19. Sumagin R, Prizant H, Lomakina E, Waugh RE, Sarelius IH. LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J. Immunol. 185(11), 7057-7066 (2010).
20. Wang S, Voisin MB, Larbi KY et al. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J. Exp. Med. 203(6), 1519-1532 (2006).
21. Kirkham PA, Barnes PJ. Oxidative stress in COPD. Chest 144(1), 266-273 (2013).
22. Lee WL, Harrison RE, Grinstein S. Phagocytosis by neutrophils. Microbes Infect. 5(14), 1299-1306 (2003).
23. McKenzie SE and Schreiber AD. Fcgamma receptors in phagocytes. Curr. Opin. Hematol. 5(1), 16-21 (1998).
24. Greenberg S and Grinstein S. Phagocytosis and innate immunity. Curr. Opin. Immunol. 14(1), 136-145 (2002).
25. Kiefer F, Brumell J, Al-Alawi N et al. The Syk protein tyrosine kinase is essential for Fcgamma receptor signaling in macrophages and neutrophils. Mol. Cell. Biol. 18(7), 4209-4220 (1998).
26. Stendahl O, Krause KH, Krischer J et al. Redistribution of intracellular Ca2+ stores during phagocytosis in human neutrophils. Science 265(5177), 1439-1441 (1994).
27. Lundqvist-Gustafsson H, Gustafsson M, Dahlgren C. Dynamic Ca2+changes in neutrophil phagosomes a source for intracellular Ca2+during phagolysosome formation? Cell Calcium 27(6), 353-362 (2000).
28. Blackwood RA, Ernst JD. Characterization of Ca2(+)-dependent phospholipid binding, vesicle aggregation and membrane fusion by annexins. Biochem. J. 266(1), 195-200 (1990).
29. Sengelov H, Kjeldsen L, Borregaard N. Control of exocytosis in early neutrophil activation. J. Immunol. 150(4), 1535-1543 (1993).
30. Segal AW. The NADPH oxidase of phagocytic cells is an electron pump that alkalinises the phagocytic vacuole. Protoplasma 184, 86-103 (1995).
31. Klebanoff SJ. Myeloperoxidase. Proc. Assoc. Am. Physicians 111(5), 383-389 (1999).
32. Rice WG, Ganz T, Kinkade JMJ, Selsted ME, Lehrer RI, Parmley RT. Defensin-rich dense granules of human neutrophils. Blood 70(3), 757-765 (1987).
33. Ganz T, Selsted ME, Szklarek D et al. Defensins. Natural peptide antibiotics of human neutrophils. J. Clin. Invest. 76(4), 1427-1435 (1985).
34. Daher KA, Selsted ME, Lehrer RI. Direct inactivation of viruses by human granulocyte defensins. J. Virol. 60(3), 1068-1074 (1986).
35. Lehrer RI, Ganz T, Szklarek D, Selsted ME. Modulation of the in vitro candidacidal activity of human neutrophil defensins by target cell metabolism and divalent cations. J. Clin. Invest. 81(6), 1829-1835 (1988).
36. Wimley WC, Selsted ME, White SH. Interactions between human defensins and lipid bilayers: Evidence for formation of multimeric pores. Prot. Sci. 3(9), 1362-1373 (1994).
37. Territo MC, Ganz T, Selsted ME, Lehrer R. Monocyte-chemotactic activity of defensins from human neutrophils. J. Clin. Invest. 84(6), 2017-2020 (1989).
38. Yang D, Chen Q, Chertov O, Oppenheim JJ. Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J. Leukoc. Biol. 68(1), 9-14 (2000).
39. Van Overveld FJ, Hiemstra PS, De Backer WA, Vermeire PA. Human mast cells can be activated by defensins. Eur. Respir. J. 8(Suppl. 19), 534s (1995).
40. Faurschou M, Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5(14), 1317-1327 (2003).
41. Campanelli D, Melchior M, Fu Y et al. Cloning of cDNA for proteinase 3: a serine protease, antibiotic, and autoantigen from human neutrophils. J. Exp. Med. 172(6), 1709-1715 (1990).
42. Salvesen G, Farley D, Shuman J, Przybyla A, Reily C, Travis J. Molecular cloning of human cathepsin G: structural similarity to mast cell and cytotoxic T lymphocyte proteinases. Biochemistry 26(8), 2289-2293 (1987).
43. Sinha S, Watorek W, Karr S, Giles J, Bode W, Travis J. Primary structure of human neutrophil elastase. Proc. Natl Acad. Sci. 84(8), 2228-2232 (1987).
44. Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P, Halbwachs-Mecarelli L. Neutrophils: molecules, functions and pathophysiological aspects. Lab. Invest. 80(5), 617-653 (2000).
45. Sengelov H, Follin P, Kjeldsen L, Lollike K, Dahlgren C, Borregaard N. Mobilization of granules and secretory vesicles during in vivo exudation of human neutrophils. J. Immunol. 154(8), 4157-4165 (1995).
46. Canonne-Hergaux F, Calafat J, Richer E et al. Expression and subcellular localization of NRAMP1 in human neutrophil granules. Blood 100(1), 268-275 (2002).
47. Kjeldsen L, Bjerrum OW, Askaa J, Borregaard N. Subcellular localization and release of human neutrophil gelatinase, confirming the existence of separate gelatinase-containing granules. Biochem. J. 287(2), 603-610 (1992).
48. Kang T, Yi J, Guo A et al. Subcellular distribution and cytokine-and chemokineregulated secretion of leukolysin/MT6- MMP/MMP-25 in neutrophils. J. Biol. Chem. 276(24), 21960-21968 (2001).
49. Delclaux C, Delacourt C, D'Ortho MP, Boyer V, Lafuma C, Harf A. Role of gelatinase B and elastase in human polymorphonuclear neutrophil migration across basement membrane. Am. J. Respir. Cell Mol. Biol. 14(3), 288-295 (1996).
50. Murphy C, Reynold JJ, Bretz U, Baggiolini M. Collagenase is a component of the specific granules of human neutrophil leukocytes. Biochem. J. 162(1), 195-197 (1977).
51. Masson PL, Heremans JF, Schonne E. Lactoferrin, an iron-binding protein in neutrophilic leukocytes. J. Exp. Med. 130(3), 643-658 (1969).
52. Oram JD and Reiter B. Inhibition of bacteria by lactoferrin and other iron-chelating agents. Biochim. Biophys. Acta 170(2), 351-365 (1968).
53. Chapple DS, Mason DJ, Joannou CL, Odell EW, Gant V, Evans RW. Structure-function relationship of antibacterial synthetic peptides homologous to a helical surface region on human lactoferrin against Escherichia coli Serotype O111. Infect. Immun. 66(6), 2434-2440 (1998).
54. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell 10(5), 1033-1043 (2002).
55. Larrick JW, Hirata M, Balint RF, Lee J, Zhong H, Wright SC. Human CAP18: a novel antimicrobial lipopolysaccharide-binding protein. Infect. Immun. 63(4), 1291-1297 (1995).
56. De Y, Chen Q, Schmidt AP et al. Ll-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T Cells. J. Exp. Med. 192(7), 1069-1074 (2000).
57. Cowland JB, Borregaard N. The individual regulation of granule protein mRNA levels during neutrophil maturation explains the heterogeneity of neutrophil granules. J. Leukoc. Biol. 66(6), 989-995 (1999).
58. Takada K, Ohno N, Yadomae T. Binding of lysozyme to lipopolysaccharide suppresses tumor necrosis factor production in vivo. Infect. Immun. 62(4), 1171-1175 (1994).
59. Cheng OZ, Palaniyar N. NET balancing: a problem in inflammatory lung diseases. Front Immunol. 4, 1 (2013).
60. Caudrillier A, Kessenbrock K, Gilliss BM et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J. Clin. Invest 122(7), 2661-2671 (2012).
61. Barnes PJ. Chronic obstructive pulmonary disease. N. Engl. J. Med. 343(4), 269-280 (2000).
62. Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol. Rev. 87(3), 1047-1082 (2007).
63. From the Global Strategy for the Diagnosis, Management and Prevention of COPD. In: Global Initiative for Chronic Obstructive Lung Disease (GOLD) (2013).
64. Decramer M, Rutten-van Mölken M, Dekhuijzen PN et al. Effects of N-acetylcysteine on outcomes in chronic obstructive pulmonary disease (Bronchitis Randomized on NAC Cost-Utility S tudy, BRONCUS): a randomised placebo-controlled trial. Lancet 365(9470), 1552-1560 (2005).
65. Liou TG, Campbell EJ. Quantum proteolysis resulting from release of single granules by human neutrophils: a novel, nonoxidative mechanism of extracellular proteolytic activity. J. Immunol. 157(6), 2624-2631 (1996).
66. Blanc PD, Thorén K. Occupation in chronic obstructive pulmonary disease and chronic bronchitis: an update [State of the Art Series. Occupational lung disease in high- and low-income countries, Edited by M. Chan-Yeung. Number 2 in the series]. Int. J. Tuberc. Lung Dis. 11(3), 251-257 (2007).
67. Caramori G, Pandit A, Papi A. Is there a difference between chronic airway inflammation in chronic severe asthma and chronic obstructive pulmonary disease? Curr. Opin. Allergy Clin. Immunol. 5(1), 77-83 (2005).
68. Almansa R, Socias L, Sanchez-Garcia M et al. Critical COPD respiratory illness is linked to increased transcriptomic activity of neutrophil proteases genes. BMC Res. Notes 5, 401 (2012).
69. Brown V, Elborn JS, Bradley J, Ennis M. Dysregulated apoptosis and NFkappaB expression in COPD subjects. Respir. Res. 10, 24 (2009).
70. Langereis J, Schweizer R, Lammers JW, Koenderman L, Ulfman L. A unique protein profile of peripheral neutrophils from COPD patients does not reflect cytokine-induced protein profiles of neutrophils in vitro. BMC Pulm. Med. 11, 44 (2011).
71. Blidberg K, Palmberg L, Dahlén B, Lantz AS, Larsson K. Chemokine release by neutrophils in chronic obstructive pulmonary disease. Innate Immun. 18(3), 503-510 (2012).
72. Perng DW, Huang HY, Chen HM, Lee YC, Perng RP. Characteristics of airway inflammation and bronchodilator reversibility in COPD: a potential guide to treatment. Chest 126(2), 375-381 (2004).
73. Coxon A, Tang T, Mayadas TN. Cytokine-activated endothelial cells delay neutrophil apoptosis in vitro and in vivo: a role for granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 190(7), 923-934 (1999).
74. Zhang J, He J, Xia J, Chen Z, Chen X. Delayed apoptosis by neutrophils from COPD patients is associated with altered bak, bcl-xl, and mcl-1 mRNA expression. Diagn. Pathol. 7, 65 (2012).
75. Braber S, Thio M, Blokhuis BR et al. An association between neutrophils and immunoglobulin free light chains in the pathogenesis of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 185(8), 817-824 (2012).
76. Moretto N, Bertolini S, Iadicicco C et al. Cigarette smoke and its component acrolein augment IL-8/CXCL8 mRNA stability via p38 MAPK/MK2 signaling in human pulmonary cells. Am. J. Physiol.Lung Cell. Mol. Physiol. 303(10), L929-L938 (2012).
77. Blidberg K, Palmberg L, Dahlén B, Lantz AS, Larsson K. Increased neutrophil migration in smokers with or without chronic obstructive pulmonary disease. Respirology 17(5), 854-860 (2012).
78. Tanni S, Pelegrino N, Angeleli A, Correa C, Godoy I. Smoking status and tumor necrosis factor-alpha mediated systemic inflammation in COPD patients. J. Inflamm. (Lond) 7, 29 (2010).
79. Nick JA, Young SK, Arndt PG et al. Selective suppression of neutrophil accumulation in ongoing pulmonary inflammation by systemic inhibition of p38 mitogen-activated protein kinase. J. Immunol. 169(9), 5260-5269 (2002).
80. Renda T, Baraldo S, Pelaia G et al. Increased activation of p38 MAPK in COPD. Eur. Respir. J. 31(1), 62-69 (2008).
81. Hope HR, Anderson GD, Burnette BL et al. Anti-inflammatory properties of a novel N-phenyl pyridinone inhibitor of p38 mitogen-activated protein kinase: preclinical-to-clinical translation. J. Pharmacol. Exp. Ther. 331(3), 882-895 (2009).
82. Banerjee A, Koziol-White C, Panettieri Jr R. p38 MAPK inhibitors, IKK2 inhibitors, and TNFa inhibitors in COPD. Curr. Opin. Pharmacol. 12(3), 287-292 (2012).
83. Beinke S, Ley SC. Functions of NF-kappaB1 and NF-kappaB2 in immune cell biology. Biochem. J. 382(2), 393-409 (2004).
84. Langereis JD, Raaijmakers HAJA, Ulfman LH, Koenderman L. Abrogation of NF-kB signaling in human neutrophils induces neutrophil survival through sustained p38-MAPK activation. J. Leukoc. Biol. 88(4), 655-664 (2010).
85. Baglole CJ, Maggirwar SB, Gasiewicz TA, Thatcher TH, Phipps RP, Sime PJ. The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-kB family member RelB. J. Biol. Chem. 283(43), 28944-28957 (2008).
86. McMillan DH, Baglole CJ, Thatcher TH, Maggirwar S, Sime PJ, Phipps RP. Lung-targeted overexpression of the NF-kappaB member RelB inhibits cigarette smoke-induced inflammation. Am. J. Pathol. 179(1), 125-133 (2011).
87. Van den Steen PE, Proost P, Wuyts A, Van Damme J, Opdenakker G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-a and leaves RANTES and MCP-2 intact. Blood 96(8), 2673-2681 (2000).
88. Beeh KM, Beier J, Kornmann O, Micke P, Buhl R. Sputum levels of metalloproteinase-9 and tissue inhibitor of metalloproteinase-1, and their ratio correlate with airway obstruction in lung transplant recipients: relation to tumor necrosis factor-a and interleukin-10. J. Heart Lung Transplant. 20(11), 1144-1151 (2001).
89. Atkinson JJ and Senior RM. Matrix metalloproteinase-9 in lung remodeling. Am. J. Respir. Cell Mol. Biol. 28(1), 12-24 (2003).
90. Gaffey K, Reynolds S, Plumb J, Kaur M, Singh D. Increased phosphorylated p38 mitogen activated protein kinase in COPD lungs. Eur. Respir. J. 42(1), 28-41 (2012).
91. Betsuyaku T, Michael Shipley J, Liu Z, Senior RM. Neutrophil emigration in the lungs, peritoneum, and skin does not require gelatinase B. Am. J. Respir. Cell Mol. Biol. 20(6), 1303-1309 (1999).
92. Corbel M, Lanchou J, Germain N, Malledant Y, Boichot E, Lagente V. Modulation of airway remodeling-associated mediators by the antifibrotic compound, pirfenidone, and the matrix metalloproteinase inhibitor, batimastat, during acute lung injury in mice. Eur. J. Pharmacol. 426(1-2), 113-121 (2001).
93. Warner RL, Beltran L, Younkin EM et al. Role of stromelysin 1 and gelatinase B in experimental acute lung injury. Am. J. Respir. Cell Mol. Biol. 24(5), 537-544 (2001).
94. Xin XF, Zhao M, Li ZL, Song Y, Shi Y. Metalloproteinase-9/tissue inhibitor of metalloproteinase-1 in induced sputum in patients with asthma and chronic obstructive pulmonary disease and their relationship to airway inflammation and airflow limitation. Zhonghua Jie He He Hu Xi Za Zhi 30(3), 192-196 (2007).
95. Overbeek SA, Braber S, Koelink PJ et al. Cigarette smoke-induced collagen destruction; key to chronic neutrophilic airway inflammation? PLoS ONE 8(1), 55612 (2013).
96. Mercer PF, Shute JK, Bhowmik A, Donaldson GC, Wedzicha JA, Warner JA. MMP-9, TIMP-1 and inflammatory cells in sputum from COPD patients during exacerbation. Respir. Res. 6, 151 (2005).
97. Carter RI, Ungurs MJ, Mumford RA, Stockley RA. Aa-Val360: a marker of neutrophil elastase and COPD disease activity. Eur. Respir. J. 41(1), 31-38 (2012).
98. Owen CA, Campbell MA, Sannes PL, Boukedes SS, Campbell EJ. Cell surface-bound elastase and cathepsin G on human neutrophils: a novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteinases. J. Cell Biol. 131(3), 775-789 (1995).
99. Kim S, Nadel JA. Role of neutrophils in mucus hypersecretion in COPD and implications for therapy. Treat. Respir. Med. 3(3), 147-159 (2004).
100. Vlahos R, Wark PAB, Anderson GP, Bozinovski S. Glucocorticosteroids differentially regulate MMP-9 and neutrophil elastase in COPD. PLoS ONE 7(3), e33277 (2012).
101. Gaggar A, Li Y, Weathington N et al. Matrix metalloprotease-9 dysregulation in lower airway secretions of cystic fibrosis patients. Am. J. Physiol. Lung Cell. Mol. Physiol. 293(1), L96-L104 (2007).
102. Sommerhoff CP, Nadel JA, Basbaum CB, Caughey GH. Neutrophil elastase and cathepsin G stimulate secretion from cultured bovine airway gland serous cells. J. Clin. Invest. 85(3), 682-689 (1990).
103. Turino GM, Ma S, Lin YY, Cantor JO, Luisetti M. Matrix elastin. Am. J. Respir. Crit. Care Med. 184(6), 637-641 (2011).
104. Barnes PJ. New concepts in chronic obstructive pulmonary disease. Annu. Rev. Med. 54(1), 113-129 (2003).
105. Stanojkovic I, Kotur-Stevuljevic J, Milenkovic B et al. Pulmonary function, oxidative stress and inflammatory markers in severe COPD exacerbation. Respir. Med. 105(Suppl. 1), S31-S37 (2011).
106. Thimmulappa RK, Gang X, Kim JH, Sussan TE, Witztum JL, Biswal S. Oxidized phospholipids impair pulmonary antibacterial defenses: evidence in mice exposed to cigarette smoke. Biochem. Biophys. Res. Commun. 426(2), 253-259 (2012).
107. Biljak VR, Rumora L, Cepelak I et al. Glutathione cycle in stable chronic obstructive pulmonary disease. Cell Biochem. Funct. 28(6), 448-453 (2010).
108. Biswas S, Hwang JW, Kirkham PA, Rahman I. Pharmacological and dietary antioxidant therapies for chronic obstructive pulmonary disease. Curr. Med. Chem. 20(12), 1496-1530 (2013).
109. Barnes PJ. New anti-inflammatory targets for chronic obstructive pulmonary disease. Nat. Rev. Drug Discov. 12(7), 543-559 (2013).
110. Radomska-Lesniewska DM, Sadowska AM, Van Overveld FJ, Demkow U, Zielinski J, De Backer WA. Influence of N-acetylcysteine on ICAM-1 expression and IL-8 release from endothelial and epithelial cells. J. Physiol. Pharmacol. 57(Suppl. 57), 325-334 (2006).
111. Decramer M, Janssens W. Mucoactive therapy in COPD. Eur. Respir. Rev. 19(116), 134-140 (2010).
112. Xu Y, Li H, Bajrami B et al. Cigarette smoke (CS) and nicotine delay neutrophil spontaneous death via suppressing production of diphosphoinositol pentakisphosphate. Proc. Natl Acad. Sci. USA 110(19), 7726-7731 (2013).
113. Altose MD. Approaches to slowing the progression of COPD. Curr. Opin. Pulm. Med. 9(2), 125-130 (2003).
114. Jen R, Rennard SI, Sin DD. Effects of inhaled corticosteroids on airway inflammation in chronic obstructive pulmonary disease: a systematic review and meta-analysis. Int. J. Chron. Obstr. Pulm. Dis. 7, 587-595 (2012).
115. O'Donnell R, Breen D, Wilson S, Djukanovic R. Inflammatory cells in the airways in COPD. Thorax 61(5), 448-454 (2006).
116. Ito K, Ito M, Elliott WM et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N. Engl. J. Med. 352(19), 1967-1976 (2005).
117. Barnes PJ. Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 131(3), 636-645 (2013).
118. Ryder MI. Nicotine effects on neutrophil F-actin formation and calcium release: implications for tobacco use and pulmonary diseases. Exp. Lung Res. 20(4), 283-296 (1994).
119. Gross NJ. Novel antiinflammatory therapies for COPD. Chest 142(5), 1300-1307 (2012).
120. Lahousse L, Loth DW, Joos GF et al. Statins, systemic inflammation and risk of death in COPD: the Rotterdam study. Pulm. Pharmacol. Ther. 26(2), 212-217 (2013).
121. Brebner JA, Stockley RA. Recent advances in alpha-1-antitrypsin deficiency-related lung disease. Expert. Rev. Respir. Med. 7(3), 213-229 (2013).
122. Beghe B, Rabe KF, Fabbri LM. Phosphodiesterase-4 inhibitor therapy for lung diseases. Am. J. Respir. Crit Care Med. 188(3), 271-278 (2013).
123. Yao GY, Ma YL, Zhang MQ, Gao ZC. Macrolide therapy decreases chronic obstructive pulmonary disease exacerbation: a meta-analysis. Respiration 86(3), 254-260 (2013).
124. Mahler DA, Huang S, Tabrizi M, Bell GM. Efficacy and safety of a monoclonal antibody recognizing interleukin-8 in COPD: a pilot study. Chest 126(3), 926-934 (2004).
125. Freeman CM, Martinez FJ, Han MK et al. Lung CD8+ T cells in COPD have increased expression of bacterial TLRs. Respir. Res. 14, 13 (2013).
126. Hanson C, Rutten EP, Wouters EF, Rennard S. Diet and vitamin D as risk factors for lung impairment and COPD. Transl. Res. 162(4), 219-236 (2013).
127. Lea S, Plumb J, Metcalfe H et al. The effect of PPAR-gamma ligands on in vitro and in vivo models of COPD. Eur. Respir. J. doi:10.1183/09031936.00187812 (2013) (Epub ahead of print).
128. Sriskantharajah S, Hamblin N, Worsley S, Calver AR, Hessel EM, Amour A. Targeting phosphoinositide 3-kinase d for the treatment of respiratory diseases. Ann. NY Acad. Sci. 1280(1), 35-39 (2013).
129. Millan DS. What is the potential for inhaled p38 inhibitors in the treatment of chronic obstructive pulmonary disease? Future Med. Chem. 3(13), 1635-1645 (2011).
130. Sydlik U, Peuschel H, Paunel-Görgülü A et al. Recovery of neutrophil apoptosis by ectoine: a new strategy against lung inflammation. Eur. Respir. J. 41(2), 433-442 (2013).