References
- Tzortzaki EG, Papi A, Neofytou E, et al. Immune and genetic mechanisms in COPD: possible targets for therapeutic interventions. Curr Drug Targets. 2013;14(2):141–148. DOI:https://doi.org/10.2174/1389450111314020002
- Morimoto K, Janssen WJ, Terada M. Defective efferocytosis by alveolar macrophages in IPF patients. Respir Med. 2012;106(12):1800–1803. DOI:https://doi.org/10.1016/j.rmed.2012.08.020
- Yun JH, Henson PM, Tuder RM. Phagocytic clearance of apoptotic cells: role in lung disease. Expert Rev Respir Med. 2008;2(6):753–765. DOI:https://doi.org/10.1586/17476348.2.6.753
- Henson PM, Vandivier RW, Douglas IS. Cell death, remodeling, and repair in chronic obstructive pulmonary disease?Proc Am Thorac Soc. 2006;3(8):713–717. DOI:https://doi.org/10.1513/pats.200605-104SF
- Mahida RY, Scott A, Parekh D, et al. Acute respiratory distress syndrome is associated with impaired alveolar macrophage efferocytosis. Eur Respir J. 2021; DOI:https://doi.org/10.1183/13993003.00829-2021
- Society AT. Standards for the diagnosis and care of subjects withchronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1995;152:S77–S121.
- Demedts IK, Demoor T, Bracke KR, et al. Role of apoptosis in the pathogenesis of COPD and pulmonary emphysema. Respir Res. 2006;7:53. DOI:https://doi.org/10.1186/1465-9921-7-53
- Müller T, Gebel S. The cellular stress response induced by aqueous extracts of cigarette smoke is critically dependent on the intracellular glutathione concentration. Carcinogenesis. 1998;19:797–801.
- Salvi SS, Barnes PJ. Chronic obstructive pulmonary disease in non-smokers. The Lancet. 2009;374(9691):733–743. DOI:https://doi.org/10.1016/S0140-6736(09)61303-9
- Lakshmi SP, Reddy AT, Reddy RC. Emerging pharmaceutical therapies for COPD. Int J Chron Obstruct Pulmon Dis. 2017;12:2141–2156. DOI:https://doi.org/10.2147/COPD.S121416
- Geraghty P, Hardigan A, Foronjy RF. Cigarette smoke activates the proto-oncogene c-src to promote airway inflammation and lung tissue destruction. Am J Respir Cell Mol Biol. 2014;50(3):559–570. DOI:https://doi.org/10.1165/rcmb.2013-0258OC
- Churg A, Zhou S, Wright JL. Series “matrix metalloproteinases in lung health and disease”: matrix metalloproteinases in COPD. Eur Respir J. 2012;39(1):197–209. DOI:https://doi.org/10.1183/09031936.00121611
- Kraen M, Frantz S, Nihlen U, et al. Matrix metalloproteinases in COPD and atherosclerosis with emphasis on the effects of smoking. PLoS One. 2019;14(2):e0211987. DOI:https://doi.org/10.1371/journal.pone.0211987
- Ilumets H, Rytila P, Demedts I, et al. Matrix metalloproteinases -8, -9 and -12 in smokers and patients with stage 0 COPD. Int J Chron Obstruct Pulmon Dis. 2007;2:369–379.
- Tilley AE, Harvey BG, Heguy A, et al. Down-regulation of the notch pathway in human airway epithelium in association with smoking and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2009;179(6):457–466. DOI:https://doi.org/10.1164/rccm.200705-795OC
- Hansson EM, Lendahl U, Chapman G. Notch signaling in development and disease. Semin Cancer Biol. 2004;14(5):320–328.
- Harper J, Yuan J, Tan J, et al. Notch signaling in development and disease. Clin Genet. 2003;64(6):461–472. DOI:https://doi.org/10.1046/j.1399-0004.2003.00194.x
- Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science. 1999;284(5415):770–776. DOI:https://doi.org/10.1126/science.284.5415.770
- Holgate ST. Epithelial damage and response. Clin Exp Allergy. 2000;30(Suppl 1):37–41. DOI:https://doi.org/10.1046/j.1365-2222.2000.00095.x
- Knight DA, Holgate ST. The airway epithelium: structural and functional properties in health and disease. Respirology. 2003;8(4):432–446. DOI:https://doi.org/10.1046/j.1440-1843.2003.00493.x
- Polosukhin VV, Lawson WE, Milstone AP, et al. Association of progressive structural changes in the bronchial epithelium with subepithelial fibrous remodeling: a potential role for hypoxia. Virchows Arch. 2007;451(4):793–803. DOI:https://doi.org/10.1007/s00428-007-0469-5
- Yu H, Li Q, Kolosov VP, et al. Regulation of cigarette smoke-mediated mucin expression by hypoxia-inducible factor-1α via epidermal growth factor receptor-mediated signaling pathways. J Appl Toxicol. 2012;32(4):282–292. DOI:https://doi.org/10.1002/jat.1679
- Polosukhin VV, Cates JM, Lawson WE, et al. Hypoxia-inducible factor-1 signalling promotes goblet cell hyperplasia in airway epithelium. J Pathol. 2011;224(2):203–211. DOI:https://doi.org/10.1002/path.2863
- Hodge S, Hodge G, Ahern J, et al. Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2007;37(6):748–755. DOI:https://doi.org/10.1165/rcmb.2007-0025OC
- Richens TR, Linderman DJ, Horstmann SA, et al. Cigarette smoke impairs clearance of apoptotic cells through oxidant-dependent activation of RhoA. Am J Respir Crit Care Med. 2009;179(11):1011–1021. DOI:https://doi.org/10.1164/rccm.200807-1148OC
- Noda N, Matsumoto K, Fukuyama S, et al. Cigarette smoke impairs phagocytosis of apoptotic neutrophils by alveolar macrophages via inhibition of the histone deacetylase/rac/CD9 pathways. Int Immunol. 2013;25(11):643–650. DOI:https://doi.org/10.1093/intimm/dxt033
- Hodge S, Hodge G, Scicchitano R, et al. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol Cell Biol. 2003;81(4):289–296. DOI:https://doi.org/10.1046/j.1440-1711.2003.t01-1-01170.x
- Hodge S, Jersmann H, Reynolds PN. The effect of colonization with potentially pathogenic microorganisms on efferocytosis in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2016;194(7):912–915. DOI:https://doi.org/10.1164/rccm.201601-0019LE
- Phipps JC, Aronoff DM, Curtis JL, et al. Cigarette smoke exposure impairs pulmonary bacterial clearance and alveolar macrophage complement-mediated phagocytosis of Streptococcus pneumoniae. Infect Immun. 2010;78(3):1214–1220. DOI:https://doi.org/10.1128/IAI.00963-09
- Tajbakhsh A, Rezaee M, Barreto GE, et al. The role of nuclear factors as “Find-Me”/alarmin signals and immunostimulation in defective efferocytosis and related disorders. Int Immunopharmacol. 2020;80:106134. DOI:https://doi.org/10.1016/j.intimp.2019.106134
- Tajbakhsh A, Bianconi V, Pirro M, et al. Efferocytosis and atherosclerosis: regulation of phagocyte function by MicroRNAs. Trends Endocrinol Metab. 2019;30(9):672–683. DOI:https://doi.org/10.1016/j.tem.2019.07.006
- Kazeros A, Harvey BG, Carolan BJ, et al. Overexpression of apoptotic cell removal receptor MERTK in alveolar macrophages of cigarette smokers. Am J Respir Cell Mol Biol. 2008;39(6):747–757. DOI:https://doi.org/10.1165/rcmb.2007-0306OC
- Subramaniam R, Mukherjee S, Chen H, et al. Restoring cigarette smoke-induced impairment of efferocytosis in alveolar macrophages. Mucosal Immunol. 2016;9(4):873–883. DOI:https://doi.org/10.1038/mi.2015.120
- Ween MP, Hamon R, Macowan MG, et al. Effects of E-cigarette E-liquid components on bronchial epithelial cells: demonstration of dysfunctional efferocytosis. Respirology. 2020;25(6):620–628. DOI:https://doi.org/10.1111/resp.13696
- Lea S, Plumb J, Metcalfe H, et al. The effect of peroxisome proliferator-activated receptor-γ ligands on in vitro and in vivo models of COPD. Eur Respir J. 2014;43(2):409–420. DOI:https://doi.org/10.1183/09031936.00187812
- Zhang S, Xie JG, Su BT, et al. MFG-E8, a clearance glycoprotein of apoptotic cells, as a new marker of disease severity in chronic obstructive pulmonary disease. Braz J Med Biol Res. 2015;48(11):1032–1038. DOI:https://doi.org/10.1590/1414-431x20154730
- Tran HB, Barnawi J, Ween M, et al. Cigarette smoke inhibits efferocytosis via deregulation of sphingosine kinase signaling: reversal with exogenous S1P and the S1P analogue FTY720. J Leukoc Biol. 2016;100(1):195–202. DOI:https://doi.org/10.1189/jlb.3A1015-471R
- Pappas K, Papaioannou AI, Kostikas K, et al. The role of macrophages in obstructive airways disease: chronic obstructive pulmonary disease and asthma. Cytokine. 2013;64(3):613–625. DOI:https://doi.org/10.1016/j.cyto.2013.09.010
- Chen YC, Lin MC, Lee CH, et al. Defective formyl peptide receptor 2/3 and annexin A1 expressions associated with M2a polarization of blood immune cells in patients with chronic obstructive pulmonary disease. J Transl Med. 2018;16(1):69. DOI:https://doi.org/10.1186/s12967-018-1435-5
- Tajbakhsh A, Gheibi Hayat SM, Butler AE, et al. Effect of soluble cleavage products of important receptors/ligands on efferocytosis: their role in inflammatory, autoimmune and cardiovascular disease. Ageing Res Rev. 2019;50:43–57. DOI:https://doi.org/10.1016/j.arr.2019.01.007
- Tajbakhsh A, Farahani N, Gheibihayat SM, et al. Autoantigen-specific immune tolerance in pathological and physiological cell death: nanotechnology comes into view. Int Immunopharmacol. 2021; 90:107177. DOI:https://doi.org/10.1016/j.intimp.2020.107177
- Eltboli O, Bafadhel M, Hollins F, et al. COPD exacerbation severity and frequency is associated with impaired macrophage efferocytosis of eosinophils. BMC Pulm Med. 2014;14(1):112. DOI:https://doi.org/10.1186/1471-2466-14-112
- Tajbakhsh A, Gheibi Hayat SM, Movahedpour A, et al. The complex roles of efferocytosis in cancer development, metastasis, and treatment. Biomed Pharmacother. 2021;140:111776. DOI:https://doi.org/10.1016/j.biopha.2021.111776
- Tajbakhsh A, Read M, Barreto GE, et al. Apoptotic neurons and amyloid-beta clearance by phagocytosis in Alzheimer’s disease: pathological mechanisms and therapeutic outlooks. Eur J Pharmacol. 2021;895:173873. DOI:https://doi.org/10.1016/j.ejphar.2021.173873
- Nakamura Y, Romberger DJ, Tate L, et al. Cigarette smoke inhibits lung fibroblast proliferation and chemotaxis. Am J Respir Crit Care Med. 1995;151(5):1497–1503. DOI:https://doi.org/10.1164/ajrccm.151.5.7735606
- Rennard SI, Togo S, Holz O. Cigarette smoke inhibits alveolar repair: a mechanism for the development of emphysema. Proc Am Thorac Soc. 2006;3(8):703–708. DOI:https://doi.org/10.1513/pats.200605-121SF
- Serban KA, Petrusca DN, Mikosz A, et al. Alpha-1 antitrypsin supplementation improves alveolar macrophages efferocytosis and phagocytosis following cigarette smoke exposure. PLoS One. 2017;12(4):e0176073. DOI:https://doi.org/10.1371/journal.pone.0176073
- McCubbrey AL, Curtis JL. Efferocytosis and lung disease. Chest. 2013;143(6):1750–1757. DOI:https://doi.org/10.1378/chest.12-2413
- Aoshiba K, Tsuji T. Immune responses in chronic obstructive pulmonary disease. Japanese J Chest Dis. 2013;72:1315–1320.
- Dewhurst JA, Lea S, Hardaker E, et al. Characterisation of lung macrophage subpopulations in COPD patients and controls. Sci Rep. 2017;7(1):7143. DOI:https://doi.org/10.1038/s41598-017-07101-2
- Tanno A, Fujino N, Yamada M, et al. Decreased expression of a phagocytic receptor siglec-1 on alveolar macrophages in chronic obstructive pulmonary disease. Respir Res. 2020;21(1):30. DOI:https://doi.org/10.1186/s12931-020-1297-2
- Savill J, Hogg N, Ren Y, et al. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest. 1992;90(4):1513–1522. DOI:https://doi.org/10.1172/JCI116019
- Ravishankar B, Shinde R, Liu H, et al. Marginal zone CD169+ macrophages coordinate apoptotic cell-driven cellular recruitment and tolerance. Proc Natl Acad Sci USA. 2014;111(11):4215–4220. DOI:https://doi.org/10.1073/pnas.1320924111
- Barnawi J, Jersmann H, Haberberger R, et al. Reduced DNA methylation of sphingosine-1 phosphate receptor 5 in alveolar macrophages in COPD: a potential link to failed efferocytosis. Respirology. 2017;22(2):315–321. DOI:https://doi.org/10.1111/resp.12949
- Petrusca DN, Gu Y, Adamowicz JJ, et al. Sphingolipid-mediated inhibition of apoptotic cell clearance by alveolar macrophages. J Biol Chem. 2010;285(51):40322–40332. DOI:https://doi.org/10.1074/jbc.M110.137604
- Hamon R, Homan CC, Tran HB, et al. Zinc and zinc transporters in macrophages and their roles in efferocytosis in COPD. PLoS One. 2014;9(10):e110056. DOI:https://doi.org/10.1371/journal.pone.0110056
- Mathias S, Peña LA, Kolesnick RN. Signal transduction of stress via ceramide. Biochem J. 1998;335(Pt 3):465–480. DOI:https://doi.org/10.1042/bj3350465
- Hodge S, Matthews G, Mukaro V, et al. Cigarette smoke-induced changes to alveolar macrophage phenotype and function are improved by treatment with procysteine. Am J Respir Cell Mol Biol. 2011;44(5):673–681. DOI:https://doi.org/10.1165/rcmb.2009-0459OC
- Ito H, Yamashita Y, Tanaka T, et al. Cigarette smoke induces endoplasmic reticulum stress and suppresses efferocytosis through the activation of RhoA. Sci Rep. 2020;10(1):12620. DOI:https://doi.org/10.1038/s41598-020-69610-x
- Tran HB, Ahern J, Hodge G, et al. Oxidative stress decreases functional airway mannose binding lectin in COPD. PLoS One. 2014;9(6):e98571. DOI:https://doi.org/10.1371/journal.pone.0098571
- Lu W, Zheng J. The function of mucins in the COPD airway. Curr Respir Care Rep. 2013;2(3):155–166. DOI:https://doi.org/10.1007/s13665-013-0051-3
- Kuebler WM, Yang Y, Samapati R, et al. Vascular barrier regulation by PAF, ceramide, caveolae, and NO - an intricate signaling network with discrepant effects in the pulmonary and systemic vasculature. Cell Physiol Biochem. 2010;26(1):29–40. DOI:https://doi.org/10.1159/000315103
- Becker KA, Riethmüller J, Lüth A, et al. Acid sphingomyelinase inhibitors normalize pulmonary ceramide and inflammation in cystic fibrosis. Am J Respir Cell Mol Biol. 2010;42(6):716–724. DOI:https://doi.org/10.1165/rcmb.2009-0174OC
- Filosto S, Castillo S, Danielson A, et al. Neutral sphingomyelinase 2: a novel target in cigarette smoke-induced apoptosis and lung injury. Am J Respir Cell Mol Biol. 2011;44(3):350–360. DOI:https://doi.org/10.1165/rcmb.2009-0422OC
- Kusner DJ, Thompson CR, Melrose NA, et al. The localization and activity of sphingosine kinase 1 are coordinately regulated with actin cytoskeletal dynamics in macrophages. J Biol Chem. 2007;282(32):23147–23162. DOI:https://doi.org/10.1074/jbc.M700193200
- Kuehnel MP, Reiss M, Anand PK, et al. Sphingosine-1-phosphate receptors stimulate macrophage plasma-membrane actin assembly via ADP release, ATP synthesis and P2X7R activation. J Cell Sci. 2009;122(Pt 4):505–512. DOI:https://doi.org/10.1242/jcs.034207
- Barnawi J, Tran HB, Roscioli E, et al. Pro-phagocytic effects of thymoquinone on cigarette smoke-exposed macrophages occur by modulation of the sphingosine-1-phosphate signalling system. COPD. 2016;13(5):653–661. DOI:https://doi.org/10.3109/15412555.2016.1153614
- Merrill AH, Jr., Schmelz EM, Dillehay DL, et al. Sphingolipids-the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol Appl Pharmacol. 1997;142(1):208–225. DOI:https://doi.org/10.1006/taap.1996.8029
- Serban KA, Rezania S, Petrusca DN, et al. Structural and functional characterization of endothelial microparticles released by cigarette smoke. Sci Rep. 2016;6:31596. DOI:https://doi.org/10.1038/srep31596
- Petrache I, Natarajan V, Zhen L, et al. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat Med. 2005;11(5):491–498. DOI:https://doi.org/10.1038/nm1238
- Joshi PC, Mehta A, Jabber WS, et al. Zinc deficiency mediates alcohol-induced alveolar epithelial and macrophage dysfunction in rats. Am J Respir Cell Mol Biol. 2009;41(2):207–216. DOI:https://doi.org/10.1165/rcmb.2008-0209OC
- Murgia C, Grosser D, Truong-Tran AQ, et al. Apical localization of zinc transporter ZnT4 in human airway epithelial cells and its loss in a murine model of allergic airway inflammation. Nutrients. 2011;3(11):910–928. DOI:https://doi.org/10.3390/nu3110910
- Napolitano JR, Liu MJ, Bao S, et al. Cadmium-mediated toxicity of lung epithelia is enhanced through NF-κB-mediated transcriptional activation of the human zinc transporter ZIP8. Am J Physiol Lung Cell Mol Physiol. 2012;302(9):L909–18. DOI:https://doi.org/10.1152/ajplung.00351.2011
- Surolia R, Li F, Singh P, et al. Cadmium decreases macrophage effrocytosis and induces emphysema via PAD4 upregulation. TP65. TP065 Environmental Exposures and Lung Disease: American Thoracic Society. Am J Respir Crit Care Med 2021;203:A3134. DOI:https://doi.org/10.1164/ajrccm-conference.2021.203.1_MeetingAbstracts.A3134
- Slotte JP, Hedström G, Rannström S, et al. Effects of sphingomyelin degradation on cell cholesterol oxidizability and steady-state distribution between the cell surface and the cell interior. Biochim Biophys Acta. 1989;985(1):90–96. DOI:https://doi.org/10.1016/0005-2736(89)90108-9
- Chang MP, Mallet WG, Mostov KE, et al. Adaptor self‐aggregation, adaptor‐receptor recognition and binding of alpha‐adaptin subunits to the plasma membrane contribute to recruitment of adaptor (AP2) components of clathrin‐coated pits. Embo J. 1993;12(5):2169–2180. DOI:https://doi.org/10.1002/j.1460-2075.1993.tb05865.x
- Justice MJ, Petrusca DN, Rogozea AL, et al. Effects of lipid interactions on model vesicle engulfment by alveolar macrophages. Biophys J. 2014;106(3):598–609. DOI:https://doi.org/10.1016/j.bpj.2013.12.036
- Iguchi K, Hirano K, Hamatake M, et al. Phosphatidylserine induces apoptosis in adherent cells. Apoptosis. 2001;6(4):263–268. DOI:https://doi.org/10.1023/A:1011331424311
- Birge RB, Boeltz S, Kumar S, et al. Phosphatidylserine is a global immunosuppressive signal in efferocytosis, infectious disease, and cancer. Cell Death Differ. 2016;23(6):962–978. DOI:https://doi.org/10.1038/cdd.2016.11
- Tajbakhsh A, Kovanen PT, Rezaee M, et al. Regulation of efferocytosis by caspase-dependent apoptotic cell death in atherosclerosis. Int J Biochem Cell Biol. 2020;120:105684. DOI:https://doi.org/10.1016/j.biocel.2020.105684
- Tajbakhsh A, Rezaee M, Kovanen PT, et al. Efferocytosis in atherosclerotic lesions: malfunctioning regulatory pathways and control mechanisms. Pharmacol Ther. 2018;188:12–25. DOI:https://doi.org/10.1016/j.pharmthera.2018.02.003
- Neri T, Pergoli L, Petrini S, et al. Particulate matter induces prothrombotic microparticle shedding by human mononuclear and endothelial cells. Toxicol in Vitro. 2016;32:333–338. DOI:https://doi.org/10.1016/j.tiv.2016.02.001
- Myers KV, Amend SR, Pienta KJ. Targeting Tyro3, axl and MerTK (TAM receptors): implications for macrophages in the tumor microenvironment. Mol Cancer. 2019;18(1):94. DOI:https://doi.org/10.1186/s12943-019-1022-2
- Aoshiba K, Yokohori N, Nagai A. Alveolar wall apoptosis causes lung destruction and emphysematous changes. Am J Respir Cell Mol Biol. 2003;28(5):555–562. DOI:https://doi.org/10.1165/rcmb.2002-0090OC
- Minematsu N, Blumental-Perry A, Shapiro SD. Cigarette smoke inhibits engulfment of apoptotic cells by macrophages through inhibition of actin rearrangement. Am J Respir Cell Mol Biol. 2011;44(4):474–482. DOI:https://doi.org/10.1165/rcmb.2009-0463OC
- Bianchi SM, Prince LR, McPhillips K, et al. Impairment of apoptotic cell engulfment by pyocyanin, a toxic metabolite of Pseudomonas aeruginosa. Am J Respir Crit Care Med. 2008;177(1):35–43. DOI:https://doi.org/10.1164/rccm.200612-1804OC
- Ji X, Yao H, Meister M, et al. Tocotrienols: dietary supplements for chronic obstructive pulmonary disease. Antioxidants. 2021;10:883. DOI:https://doi.org/10.3390/antiox10060883
- Brown LA, Ping XD, Harris FL, et al. Glutathione availability modulates alveolar macrophage function in the chronic ethanol-fed rat. Am J Physiol Lung Cell Mol Physiol. 2007;292(4):L824–32. DOI:https://doi.org/10.1152/ajplung.00346.2006
- Dobashi K, Aihara M, Araki T, et al. Regulation of LPS induced IL-12 production by IFN-gamma and IL-4 through intracellular glutathione status in human alveolar macrophages . Clin Exp Immunol. 2001;124(2):290–296. DOI:https://doi.org/10.1046/j.1365-2249.2001.01535.x
- Rahman I, MacNee W. Oxidative stress and regulation of glutathione in lung inflammation. Eur Respir J. 2000;16(3):534–554. DOI:https://doi.org/10.1034/j.1399-3003.2000.016003534.x
- Gould NS, Min E, Huang J, et al. Glutathione depletion accelerates cigarette smoke-induced inflammation and airspace enlargement. Toxicol Sci. 2015;147(2):466–474. DOI:https://doi.org/10.1093/toxsci/kfv143
- MacKinnon AC, Farnworth SL, Hodkinson PS, et al. Regulation of alternative macrophage activation by galectin-3. J Immunol. 2008;180(4):2650–2658. DOI:https://doi.org/10.4049/jimmunol.180.4.2650
- Caberoy NB, Alvarado G, Bigcas JL, et al. Galectin-3 is a new MerTK-specific eat-me signal. J Cell Physiol. 2012;227(2):401–407. DOI:https://doi.org/10.1002/jcp.22955
- Mukaro VR, Bylund J, Hodge G, et al. Lectins offer new perspectives in the development of macrophage-targeted therapies for COPD/emphysema. PLoS One. 2013;8(2):e56147. DOI:https://doi.org/10.1371/journal.pone.0056147
- Pei C, Wang X, Lin Y, et al. Inhibition of galectin-3 alleviates cigarette smoke Extract-Induced autophagy and dysfunction in endothelial progenitor cells. Oxid Med Cell Longev. 2019;2019:7252943. DOI:https://doi.org/10.1155/2019/7252943
- Grootendorst DC, Gauw SA, Verhoosel RM, et al. Reduction in sputum neutrophil and eosinophil numbers by the PDE4 inhibitor roflumilast in patients with COPD. Thorax. 2007;62(12):1081–1087. DOI:https://doi.org/10.1136/thx.2006.075937
- Heijink IH, Pouwels SD, Leijendekker C, et al. Cigarette smoke-induced damage-associated molecular pattern release from necrotic neutrophils triggers proinflammatory mediator release. Am J Respir Cell Mol Biol. 2015;52(5):554–562. DOI:https://doi.org/10.1165/rcmb.2013-0505OC
- Vandivier RW, Henson PM, Douglas IS. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest. 2006;129(6):1673–1682. DOI:https://doi.org/10.1378/chest.129.6.1673
- van der Toorn M, Slebos DJ, de Bruin HG, et al. Critical role of aldehydes in cigarette smoke-induced acute airway inflammation. Respir Res. 2013;14(1):45. DOI:https://doi.org/10.1186/1465-9921-14-45
- Geering B, Stoeckle C, Conus S, et al. Living and dying for inflammation: neutrophils, eosinophils, basophils. Trends Immunol. 2013;34(8):398–409. DOI:https://doi.org/10.1016/j.it.2013.04.002
- Scheel-Toellner D, Wang KQ, Webb PR, et al. Early events in spontaneous neutrophil apoptosis. Biochem Soc Trans. 2004;32(Pt3):461–464. DOI:https://doi.org/10.1042/BST0320461
- Du H, Sun J, Chen Z, et al. Cigarette smoke-induced failure of apoptosis resulting in enhanced neoplastic transformation in human bronchial epithelial cells. J Toxicol Environ Health A. 2012;75(12):707–720. DOI:https://doi.org/10.1080/15287394.2012.690088
- Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol. 2008;8(4):279–289. DOI:https://doi.org/10.1038/nri2215
- Guzik K, Skret J, Smagur J, et al. Cigarette smoke-exposed neutrophils die unconventionally but are rapidly phagocytosed by macrophages. Cell Death Dis. 2011;2:e131. DOI:https://doi.org/10.1038/cddis.2011.13
- Pouwels SD, Heijink IH, ten Hacken NH, et al. DAMPs activating innate and adaptive immune responses in COPD. Mucosal Immunol. 2014;7(2):215–226. DOI:https://doi.org/10.1038/mi.2013.77
- Tait SW, Green DR. Mitochondria and cell signalling. J Cell Sci. 2012;125(Pt 4):807–815. DOI:https://doi.org/10.1242/jcs.099234
- Wen Z, Xu L, Chen X, et al. Autoantibody induction by DNA-containing immune complexes requires HMGB1 with the TLR2/microRNA-155 pathway. J Immunol. 2013;190(11):5411–5422. DOI:https://doi.org/10.4049/jimmunol.1203301
- Kunkel SL, Standiford T, Kasahara K, et al. Interleukin-8 (IL-8): the major neutrophil chemotactic factor in the lung. Exp Lung Res. 1991;17(1):17–23. DOI:https://doi.org/10.3109/01902149109063278
- Masubuchi T, Koyama S, Sato E, et al. Smoke extract stimulates lung epithelial cells to release neutrophil and monocyte chemotactic activity. Am J Pathol. 1998;153(6):1903–1912. DOI:https://doi.org/10.1016/S0002-9440(10)65704-5
- Zitvogel L, Kepp O, Kroemer G. Decoding cell death signals in inflammation and immunity. Cell. 2010;140(6):798–804. DOI:https://doi.org/10.1016/j.cell.2010.02.015
- Liu G, Wang J, Park Y-J, et al. High mobility group protein-1 inhibits phagocytosis of apoptotic neutrophils through binding to phosphatidylserine. J Immunol. 2008;181(6):4240–4246. DOI:https://doi.org/10.4049/jimmunol.181.6.4240
- Wang Y, Luo G, Chen J, et al. Cigarette smoke attenuates phagocytic ability of macrophages through down-regulating milk fat globule-EGF factor 8 (MFG-E8) expressions. Sci Rep. 2017;7:42642. DOI:https://doi.org/10.1038/srep42642
- Friggeri A, Yang Y, Banerjee S, et al. HMGB1 inhibits macrophage activity in efferocytosis through binding to the alphavbeta3-integrin. Am J Physiol Cell Physiol. 2010;299(6):C1267–C76. DOI:https://doi.org/10.1152/ajpcell.00152.2010
- Shao MX, Nadel JA. Neutrophil elastase induces MUC5AC mucin production in human airway epithelial cells via a Cascade involving protein kinase C, reactive oxygen species, and TNF-alpha-converting enzyme. J Immunol. 2005;175(6):4009–4016. DOI:https://doi.org/10.4049/jimmunol.175.6.4009
- Damiano V, Tsang A, Kucich U, et al. Immunolocalization of elastase in human emphysematous lungs. J Clin Invest. 1986;78(2):482–493. DOI:https://doi.org/10.1172/JCI112600
- Fadok VA, Warner ML, Bratton DL, et al. CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (αvβ3). J Immunol. 1998;161:6250–6257.
- Majai G, Sarang Z, Csomós K, et al. PPARgamma-dependent regulation of human macrophages in phagocytosis of apoptotic cells. Eur J Immunol. 2007;37(5):1343–1354. DOI:https://doi.org/10.1002/eji.200636398
- Asada K, Sasaki S, Suda T, et al. Antiinflammatory roles of peroxisome proliferator-activated receptor gamma in human alveolar macrophages. Am J Respir Crit Care Med. 2004;169(2):195–200. DOI:https://doi.org/10.1164/rccm.200207-740OC
- Shan M, You R, Yuan X, et al. Agonistic induction of PPARγ reverses cigarette smoke-induced emphysema. J Clin Invest. 2014;124(3):1371–1381. DOI:https://doi.org/10.1172/JCI70587
- Yoon YS, Kim SY, Kim MJ, et al. PPARγ activation following apoptotic cell instillation promotes resolution of lung inflammation and fibrosis via regulation of efferocytosis and proresolving cytokines. Mucosal Immunol. 2015;8(5):1031–1046. DOI:https://doi.org/10.1038/mi.2014.130
- Li Y, Wen X, Spataro BC, et al. Hepatocyte growth factor is a downstream effector that mediates the antifibrotic action of peroxisome proliferator-activated receptor-gamma agonists. J Am Soc Nephrol. 2006;17(1):54–65. DOI:https://doi.org/10.1681/ASN.2005030257
- Lakshmi SP, Reddy AT, Zhang Y, et al. Down-regulated peroxisome proliferator-activated receptor γ (PPARγ) in lung epithelial cells promotes a PPARγ agonist-reversible proinflammatory phenotype in chronic obstructive pulmonary disease (COPD). J Biol Chem. 2014;289(10):6383–6393. DOI:https://doi.org/10.1074/jbc.M113.536805
- Rinne ST, Liu CF, Feemster LC, et al. Thiazolidinediones are associated with a reduced risk of COPD exacerbations. Int J Chron Obstruct Pulmon Dis. 2015;10:1591–1597. DOI:https://doi.org/10.2147/COPD.S82643
- Moreira AR, Pereira de Castro TB, Kohler JB, et al. Chronic exposure to diesel particles worsened emphysema and increased M2-like phenotype macrophages in a PPE-induced model. PLoS One. 2020;15(1):e0228393. DOI:https://doi.org/10.1371/journal.pone.0228393
- Mehta M, DeekshaSharma N, et al. Interactions with the macrophages: an emerging targeted approach using novel drug delivery systems in respiratory diseases. Chem Biol Interact. 2019;304:10–19. DOI:https://doi.org/10.1016/j.cbi.2019.02.021
- Cooray SN, Gobbetti T, Montero-Melendez T, et al. Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses . Proc Natl Acad Sci USA. 2013;110(45):18232–18237. DOI:https://doi.org/10.1073/pnas.1308253110
- Maderna P, Cottell DC, Toivonen T, et al. FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J. 2010;24(11):4240–4249. DOI:https://doi.org/10.1096/fj.10-159913
- Sugimoto MA, Vago JP, Teixeira MM, et al. Annexin A1 and the resolution of inflammation: modulation of neutrophil recruitment, apoptosis, and clearance. J Immunol Res. 2016;2016:8239258. DOI:https://doi.org/10.1155/2016/8239258
- Blume KE, Soeroes S, Waibel M, et al. Cell surface externalization of annexin A1 as a failsafe mechanism preventing inflammatory responses during secondary necrosis. J Immunol. 2009;183(12):8138–8147. DOI:https://doi.org/10.4049/jimmunol.0902250
- Pupjalis D, Goetsch J, Kottas DJ, et al. Annexin A1 released from apoptotic cells acts through formyl peptide receptors to dampen inflammatory monocyte activation via JAK/STAT/SOCS signalling. EMBO Mol Med. 2011;3(2):102–114. DOI:https://doi.org/10.1002/emmm.201000113
- Filep JG. Biasing the lipoxin A4/formyl peptide receptor 2 pushes inflammatory resolution. Proc Natl Acad Sci USA. 2013;110(45):18033–18034. DOI:https://doi.org/10.1073/pnas.1317798110
- DiMasi JA. Innovating by developing new uses of already-approved drugs: trends in the marketing approval of supplemental indications. Clin Ther. 2013;35(6):808–818. DOI:https://doi.org/10.1016/j.clinthera.2013.04.004
- Mancini GB, Etminan M, Zhang B, et al. Reduction of morbidity and mortality by statins, angiotensin-converting enzyme inhibitors, and angiotensin receptor blockers in patients with chronic obstructive pulmonary disease. J Am Coll Cardiol. 2006;47(12):2554–2560. DOI:https://doi.org/10.1016/j.jacc.2006.04.039
- Søyseth V, Brekke P, Smith P, et al. Statin use is associated with reduced mortality in COPD. Eur Respir J. 2007;29(2):279–283. DOI:https://doi.org/10.1183/09031936.00106406
- Lee J-H, Lee D-S, Kim E-K, et al. Simvastatin inhibits cigarette smoking-induced emphysema and pulmonary hypertension in rat lungs. Am J Respir Crit Care Med. 2005;172(8):987–993. DOI:https://doi.org/10.1164/rccm.200501-041OC
- Wright JL, Zhou S, Preobrazhenska O, et al. Statin reverses smoke-induced pulmonary hypertension and prevents emphysema but not airway remodeling. Am J Respir Crit Care Med. 2011;183(1):50–58. DOI:https://doi.org/10.1164/rccm.201003-0399OC
- Morimoto K, Janssen WJ, Fessler MB, et al. Lovastatin enhances clearance of apoptotic cells (efferocytosis) with implications for chronic obstructive pulmonary disease. J Immunol. 2006;176(12):7657–7665. DOI:https://doi.org/10.4049/jimmunol.176.12.7657
- Janssen WJ, McPhillips KA, Dickinson MG, et al. Surfactant proteins a and D suppress alveolar macrophage phagocytosis via interaction with SIRP alpha. Am J Respir Crit Care Med. 2008;178(2):158–167. DOI:https://doi.org/10.1164/rccm.200711-1661OC
- Hodge S, Hodge G, Jersmann H, et al. Azithromycin improves macrophage phagocytic function and expression of mannose receptor in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008;178(2):139–148. DOI:https://doi.org/10.1164/rccm.200711-1666OC
- Yamaryo T, Oishi K, Yoshimine H, et al. Fourteen-Member macrolides promote the phosphatidylserine receptor-dependent phagocytosis of apoptotic neutrophils by alveolar macrophages. Antimicrob Agents Chemother. 2003;47(1):48–53. DOI:https://doi.org/10.1128/AAC.47.1.48-53.2003
- Hodge S, Hodge G, Brozyna S, et al. Azithromycin increases phagocytosis of apoptotic bronchial epithelial cells by alveolar macrophages. Eur Respir J. 2006;28(3):486–495. DOI:https://doi.org/10.1183/09031936.06.00001506
- Hodge S, Tran HB, Hamon R, et al. Nonantibiotic macrolides restore airway macrophage phagocytic function with potential anti-inflammatory effects in chronic lung diseases. Am J Physiol Lung Cell Mol Physiol. 2017;312(5):L678–L87. DOI:https://doi.org/10.1152/ajplung.00518.2016
- Stein M, Keshav S, Harris N, et al. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med. 1992;176(1):287–292. DOI:https://doi.org/10.1084/jem.176.1.287
- Murphy BS, Sundareshan V, Cory TJ, et al. Azithromycin alters macrophage phenotype. J Antimicrob Chemother. 2008;61(3):554–560. DOI:https://doi.org/10.1093/jac/dkn007
- Cory TJ. Effect of azithromycin on macrophage phenotype during pulmonary infections and cystic fibrosis. University of Kentucky; 2011.
- Macowan MG, Liu H, Keller MD, et al. Interventional low-dose azithromycin attenuates cigarette smoke-induced emphysema and lung inflammation in mice. Physiol Rep. 2020;8(13):e14419. DOI:https://doi.org/10.14814/phy2.14419
- Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2(2):107–117. DOI:https://doi.org/10.1038/35052055
- Sender V, Moulakakis C, Stamme C. Pulmonary surfactant protein a enhances endolysosomal trafficking in alveolar macrophages through regulation of Rab7. J Immunol. 2011;186(4):2397–2411. DOI:https://doi.org/10.4049/jimmunol.1002446
- Rodman JS, Wandinger-Ness A. Rab GTPases coordinate endocytosis. J Cell Sci. 2000;113 Pt 2:183–192. DOI:https://doi.org/10.1242/jcs.113.2.183
- Hart SP, Alexander KM, Dransfield I. Immune complexes bind preferentially to Fc gamma RIIA (CD32) on apoptotic neutrophils, leading to augmented phagocytosis by macrophages and release of proinflammatory cytokines. J Immunol. 2004;172(3):1882–1887. DOI:https://doi.org/10.4049/jimmunol.172.3.1882
- Brencicova E, Diebold SS. Nucleic acids and endosomal pattern recognition: how to tell friend from foe?Front Cell Infect Microbiol. 2013;3:37.
- Ivan E, Colovai AI. Human Fc receptors: critical targets in the treatment of autoimmune diseases and transplant rejections. Hum Immunol. 2006;67(7):479–491. DOI:https://doi.org/10.1016/j.humimm.2005.12.001
- Green DR, Oguin TH, Martinez J. The clearance of dying cells: table for two. Cell Death Differ. 2016;23(6):915–926. DOI:https://doi.org/10.1038/cdd.2015.172
- Henault J, Martinez J, Riggs JM, et al. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity. 2012;37(6):986–997. DOI:https://doi.org/10.1016/j.immuni.2012.09.014
- Woo CC, Kumar AP, Sethi G, et al. Thymoquinone: potential cure for inflammatory disorders and cancer. Biochem Pharmacol. 2012;83(4):443–451. DOI:https://doi.org/10.1016/j.bcp.2011.09.029