Exposure to diesel exhaust particle extracts (DEPe) impairs some polarization markers and functions of human macrophages through activation of AhR and Nrf2

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Jaguin, Marie ^a   Fardel, Olivier ^a,b   Lecureur, Valérie ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b RENNES UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CCL18 CHEMOKINE; CD200 RECEPTOR; CHEMOKINE; CHEMOKINE RECEPTOR CCR4; CYTOCHROME P450 1B1; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEME OXYGENASE 1; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MACROPHAGE DERIVED CHEMOKINE; MONOCYTE CHEMOTACTIC PROTEIN 3; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; EXHAUST GAS; INTERLEUKIN DERIVATIVE; NFE2L2 PROTEIN, HUMAN; PARTICULATE MATTER;

ARTICLE; CELL POLARITY; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; EXHAUST GAS; GENE SILENCING; HUMAN; HUMAN CELL; MACROPHAGE; MACROPHAGE FUNCTION; MONOCYTE; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; CELL DIFFERENTIATION; DRUG EFFECTS; EXOCYTOSIS; GENETICS; MACROPHAGE ACTIVATION; METABOLISM; PARTICULATE MATTER; TOXICITY;

CELL DIFFERENTIATION; CHEMOKINES; EXOCYTOSIS; HUMANS; INTERLEUKINS; MACROPHAGE ACTIVATION; MACROPHAGES; NF-E2-RELATED FACTOR 2; PARTICULATE MATTER; RECEPTORS, ARYL HYDROCARBON; VEHICLE EMISSIONS;

EID: 84923579421     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116560     Document Type: Article

References (69)

1. Miller MR, Shaw CA, Langrish JP (2012) From particles to patients: oxidative stress and the cardiovascular effects of air pollution. Future Cardiol 8: 577-602. doi: 10.2217/fca.12.43 PMID: 22871197
2. Ghio AJ, Smith CB, Madden MC (2012) Diesel exhaust particles and airway inflammation. Curr Opin Pulm Med 18: 144-150. doi: 10.1097/MCP.0b013e32834f0e2a PMID: 22234273
3. Møller P, Mikkelsen L, Vesterdal LK, Folkmann JK, Forchhammer L, et al. (2011) Hazard identification of particulate matter on vasomotor dysfunction and progression of atherosclerosis. Crit Rev Toxicol 41: 339-368. doi: 10.3109/10408444.2010.533152 PMID: 21345153
4. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3: 23-35. PMID: 12511873
5. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686. PMID: 15530839
6. Vogel CFA, Sciullo E, Wong P, Kuzmicky P, Kado N, et al. (2005) Induction of proinflammatory cytokines and C-reactive protein in human macrophage cell line U937 exposed to air pollution particulates. Environ Health Perspect 113: 1536-1541. PMID: 16263508
7. Miyata R, van Eeden SF (2011) The innate and adaptive immune response induced by alveolar macrophages exposed to ambient particulate matter. Toxicol Appl Pharmacol 257: 209-226. doi: 10.1016/j.taap.2011.09.007 PMID: 21951342
8. Amakawa K, Terashima T, Matsuzaki T, Matsumaru A, Sagai M, et al. (2003) Suppressive effects of diesel exhaust particles on cytokine release from human and murine alveolar macrophages. Exp Lung Res 29: 149-164. PMID: 12637227
9. Mundandhara SD, Becker S, Madden MC (2006) Effects of diesel exhaust particles on human alveolar macrophage ability to secrete inflammatory mediators in response to lipopolysaccharide. Toxicol Vitro 20: 614-624. PMID: 16360300
10. Sawyer K, Mundandhara S, Ghio AJ, Madden MC (2010) The effects of ambient particulate matter on human alveolar macrophage oxidative and inflammatory responses. J Toxicol Environ Health A 73: 41-57. doi: 10.1080/15287390903248901 PMID: 19953419
11. Hiura TS, Kaszubowski MP, Li N, Nel AE (1999) Chemicals in diesel exhaust particles generate reactive oxygen radicals and induce apoptosis in macrophages. J Immunol 163: 5582-5591. PMID: 10553087
12. Baulig A, Garlatti M, Bonvallot V, Marchand A, Barouki R, et al. (2003) Involvement of reactive oxygen species in the metabolic pathways triggered by diesel exhaust particles in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 285: L671-679. PMID: 12730081
13. Fardel O (2013) Cytokines as molecular targets for aryl hydrocarbon receptor ligands: implications for toxicity and xenobiotic detoxification. Expert Opin Drug Metab Toxicol 9: 141-152. doi: 10.1517/17425255.2013.738194 PMID: 23230817
14. Nguyen NT, Hanieh H, Nakahama T, Kishimoto T (2013) The roles of aryl hydrocarbon receptor in immune responses. Int Immunol 25: 335-343. doi: 10.1093/intimm/dxt011 PMID: 23580432
15. Li N, Venkatesan MI, Miguel A, Kaplan R, Gujuluva C, et al. (2000) Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. J Immunol 165: 3393-3401. PMID: 10975858
16. Li N, Alam J, Venkatesan MI, Eiguren-Fernandez A, Schmitz D, et al. (2004) Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflammatory and oxidizing effects of diesel exhaust chemicals. J Immunol 173: 3467-3481. PMID: 15322212
17. Li N, Nel AE (2006) Role of the Nrf2-mediated signaling pathway as a negative regulator of inflammation: implications for the impact of particulate pollutants on asthma. Antioxid Redox Signal 8: 88-98. PMID: 16487041
18. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, et al. (2004) Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 114: 1248-1259. PMID: 15520857
19. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, et al. (2006) Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 116: 984-995. PMID: 16585964
20. Li YJ, Takizawa H, Azuma A, Kohyama T, Yamauchi Y, et al. (2008) Disruption of Nrf2 enhances susceptibility to airway inflammatory responses induced by low-dose diesel exhaust particles in mice. Clin Immunol Orlando Fla 128: 366-373. doi: 10.1016/j.clim.2008.05.005 PMID: 18614404
21. Williams MA, Rangasamy T, Bauer SM, Killedar S, Karp M, et al. (2008) Disruption of the transcription factor Nrf2 promotes pro-oxidative dendritic cells that stimulate Th2-like immunoresponsiveness upon activation by ambient particulate matter. J Immunol 181: 4545-4559. PMID: 18802057
22. Bleck B, Tse DB, Jaspers I, Curotto de Lafaille MA, Reibman J (2006) Diesel exhaust particle-exposed human bronchial epithelial cells induce dendritic cell maturation. J Immunol 176: 7431-7437. PMID: 16751388
23. Chan RC-F, Wang M, Li N, Yanagawa Y, Onoé K, et al. (2006) Pro-oxidative diesel exhaust particle chemicals inhibit LPS-induced dendritic cell responses involved in T-helper differentiation. J Allergy Clin Immunol 118: 455-465. PMID: 16890772
24. Braun A, Bewersdorff M, Lintelmann J, Matuschek G, Jakob T, et al. (2010) Differential impact of diesel particle composition on pro-allergic dendritic cell function. Toxicol Sci 113: 85-94. doi: 10.1093/toxsci/kfp239 PMID: 19805405
25. Chaudhuri N, Jary H, Lea S, Khan N, Piddock KC, et al. (2012) Diesel exhaust particle exposure in vitro alters monocyte differentiation and function. PloS One 7: e51107. doi: 10.1371/journal.pone.0051107 PMID: 23236439
26. Van Grevenynghe J, Rion S, Le Ferrec E, Le Vee M, Amiot L, et al. (2003) Polycyclic aromatic hydrocarbons inhibit differentiation of human monocytes into macrophages. J Immunol 170: 2374-2381. PMID: 12594260
27. Martinez FO, Gordon S, Locati M, Mantovani A (2006) Transcriptional profiling of the human monocyte-to- macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177: 7303-7311. PMID: 17082649
28. World Medical Association Declaration of Helsinki (1997) Recommendations guiding physicians in biomedical research involving human subjects Cardiovasc Res 35: 2-3. PMID: 9302340
29. Moreau A, Le Vee M, Jouan E, Parmentier Y, Fardel O (2011) Drug transporter expression in human macrophages. Fundam Clin Pharmacol 25: 743-752. doi: 10.1111/j.1472-8206.2010.00913.x PMID: 21210849
30. Lecureur V, Ferrec EL, N'diaye M, Vee ML, Gardyn C, et al. (2005) ERK-dependent induction of TNFalpha expression by the environmental contaminant benzo(a)pyrene in primary human macrophages. FEBS Lett 579: 1904-1910. PMID: 15792794
31. Pi J, Bai Y, Reece JM, Williams J, Liu D, et al. (2007) Molecular mechanism of human Nrf2 activation and degradation: role of sequential phosphorylation by protein kinase CK2. Free Radic Biol Med 42: 1797-1806. PMID: 17512459
32. Hatanaka N, Yamazaki H, Kizu R, Hayakawa K, Aoki Y, et al. (2001) Induction of cytochrome P450 1B1 in lung, liver and kidney of rats exposed to diesel exhaust. Carcinogenesis 22: 2033-2038. PMID: 11751436
33. Verheyen GR, Nuijten J-M, Van Hummelen P, Schoeters GR (2004) Microarray analysis of the effect of diesel exhaust particles on in vitro cultured macrophages. Toxicol Vitro 18: 377-391. PMID: 15046786
34. Jaguin M, Houlbert N, Fardel O, Lecureur V (2013) Polarization profiles of human M-CSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell Immunol 281: 51-61. doi: 10.1016/j.cellimm.2013.01.010 PMID: 23454681
35. Ambarus CA, Krausz S, van Eijk M, Hamann J, Radstake TRDJ, et al. (2012) Systematic validation of specific phenotypic markers for in vitro polarized human macrophages. J Immunol Methods 375: 196-206. doi: 10.1016/j.jim.2011.10.013 PMID: 22075274
36. Laupeze B, Amiot L, Sparfel L, Le Ferrec E, Fauchet R, et al. (2002) Polycyclic aromatic hydrocarbons affect functional differentiation and maturation of human monocyte-derived dendritic cells. J Immunol 168: 2652-2658. PMID: 11884429
37. Kimura A, Naka T, Nakahama T, Chinen I, Masuda K, et al. (2009) Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J Exp Med 206: 2027-2035. doi: 10. 1084/jem.20090560 PMID: 19703987
38. Chao MW, Po IP, Laumbach RJ, Koslosky J, Cooper K, et al. (2012) DEP induction of ROS in capillarylike endothelial tubes leads to VEGF-A expression. Toxicology 297: 34-46. doi: 10.1016/j.tox.2012.03.009 PMID: 22507881
39. Davarinos NA, Pollenz RS (1999) Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytosplasmic proteasome following nuclear export. J Biol Chem 274: 28708-28715. PMID: 10497241
40. Gowdy KM, Krantz QT, King C, Boykin E, Jaspers I, et al. (2010) Role of oxidative stress on diesel-enhanced influenza infection in mice. Part Fibre Toxicol 7: 34. doi: 10.1186/1743-8977-7-34 PMID: 21092162
41. Yin XJ, Dong CC, Ma JYC, Roberts JR, Antonini JM, et al. (2007) Suppression of phagocytic and bactericidal functions of rat alveolar macrophages by the organic component of diesel exhaust particles. J Toxicol Environ Health A 70: 820-828. PMID: 17454558
42. Taront S, Dieudonné A, Blanchard S, Jeannin P, Lassalle P, et al. (2009) Implication of scavenger receptors in the interactions between diesel exhaust particles and immature or mature dendritic cells. Part Fibre Toxicol 6: 9. doi: 10.1186/1743-8977-6-9 PMID: 19284653
43. Salvi S, Blomberg A, Rudell B, Kelly F, Sandström T, et al. (1999) Acute inflammatory responses in the airways and peripheral blood after short-term exposure to diesel exhaust in healthy human volunteers. Am J Respir Crit Care Med 159: 702-709. PMID: 10051240
44. Stenfors N, Nordenhäll C, Salvi SS, Mudway I, Söderberg M, et al. (2004) Different airway inflammatory responses in asthmatic and healthy humans exposed to diesel. Eur Respir J 23: 82-86. PMID: 14738236
45. Chvatchko Y, Hoogewerf AJ, Meyer A, Alouani S, Juillard P, et al. (2000) A key role for CC chemokine receptor 4 in lipopolysaccharide-induced endotoxic shock. J Exp Med 191: 1755-1764. PMID: 10811868
46. De Nadaï P, Charbonnier A-S, Chenivesse C, Sénéchal S, Fournier C, et al. (2006) Involvement of CCL18 in allergic asthma. J Immunol 176: 6286-6293. PMID: 16670340
47. Chenivesse C, Chang Y, Azzaoui I, Ait Yahia S, Morales O, et al. (2012) Pulmonary CCL18 recruits human regulatory T cells. J Immunol 189: 128-137. doi: 10.4049/jimmunol.1003616 PMID: 22649201
48. Quintana FJ, Sherr DH (2013) Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol Rev 65: 1148-1161. doi: 10.1124/pr.113.007823 PMID: 23908379
49. Sparfel L, Pinel-Marie M-L, Boize M, Koscielny S, Desmots S, et al. (2010) Transcriptional signature of human macrophages exposed to the environmental contaminant benzo(a)pyrene. Toxicol Sci 114: 247-259. doi: 10.1093/toxsci/kfq007 PMID: 20064835
50. Podechard N, Lecureur V, Le Ferrec E, Guenon I, Sparfel L, et al. (2008) Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation. Toxicol Lett 177: 130-137. doi: 10.1016/j.toxlet.2008.01.006 PMID: 18289803
51. Benson JM, Shepherd DM (2011) Dietary ligands of the aryl hydrocarbon receptor induce anti-inflammatory and immunoregulatory effects on murine dendritic cells. Toxicol Sci 124: 327-338. doi: 10. 1093/toxsci/kfr249 PMID: 21948866
52. Vogel CFA, Sciullo E, Li W, Wong P, Lazennec G, et al. (2007) RelB, a new partner of aryl hydrocarbon receptor-mediated transcription. Mol Endocrinol Baltim Md 21: 2941-2955. PMID: 17823304
53. Masuda K, Kimura A, Hanieh H, Nguyen NT, Nakahama T, et al. (2011) Aryl hydrocarbon receptor negatively regulates LPS-induced IL-6 production through suppression of histamine production in macrophages. Int Immunol 23: 637-645. doi: 10.1093/intimm/dxr072 PMID: 21930594
54. N'Diaye M, Le Ferrec E, Lagadic-Gossmann D, Corre S, Gilot D, et al. (2006) Aryl hydrocarbon recep-tor- and calcium-dependent induction of the chemokine CCL1 by the environmental contaminant benzo [a]pyrene. J Biol Chem 281: 19906-19915. PMID: 16679317
55. Vogel CFA, Sciullo E, Matsumura F (2007) Involvement of RelB in aryl hydrocarbon receptor-mediated induction of chemokines. Biochem Biophys Res Commun 363: 722-726. PMID: 17900530
56. Rebourcet D, Odet F, Vérot A, Combe E, Meugnier E, et al. (2010) The effects of an in utero exposure to 2,3,7,8-tetrachloro-dibenzo-p-dioxin on male reproductive function: identification of Ccl5 as a potential marker. Int J Androl 33: 413-424. doi: 10.1111/j.1365-2605.2009.01020.x PMID: 20059583
57. Morino-Koga S, Uchi H, Tsuji G, Takahara M, Kajiwara J, et al. (2013) Reduction of CC-chemokine ligand 5 by aryl hydrocarbon receptor ligands. J Dermatol Sci 72: 9-15. doi: 10.1016/j.jdermsci.2013.04.031 PMID: 23810773
58. Kollert F, Probst C, Müller-Quernheim J, Zissel G, Prasse A (2009) CCL18 production is decreased in alveolar macrophages from cigarette smokers. Inflammation 32: 163-168. doi: 10.1007/s10753-009-9115-5 PMID: 19357939
59. Fahy O, Sénéchal S, Pène J, Scherpereel A, Lassalle P, et al. (2002) Diesel exposure favors Th2 cell recruitment by mononuclear cells and alveolar macrophages from allergic patients by differentially regulating macrophage-derived chemokine and IFN-gamma-induced protein-10 production. J Immunol 168: 5912-5919. PMID: 12023397
60. Sun YV, Boverhof DR, Burgoon LD, Fielden MR, Zacharewski TR (2004) Comparative analysis of dioxin response elements in human, mouse and rat genomic sequences. Nucleic Acids Res 32: 4512-4523. PMID: 15328365
61. Jeong S-I, Choi B-M, Jang SI (2010) Sulforaphane suppresses TARC/CCL17 and MDC/CCL22 expression through heme oxygenase-1 and NF-κB in human keratinocytes. Arch Pharm Res 33: 1867-1876. doi: 10.1007/s12272-010-1120-6 PMID: 21116791
62. Iizuka T, Ishii Y, Itoh K, Kiwamoto T, Kimura T, et al. (2005) Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema. Genes Cells Devoted Mol Cell Mech 10: 1113-1125. PMID: 16324149
63. Papaiahgari S, Yerrapureddy A, Reddy SR, Reddy NM, Dodd-O JM, et al. (2007) Genetic and pharmacologic evidence links oxidative stress to ventilator-induced lung injury in mice. Am J Respir Crit Care Med 176: 1222-1235. PMID: 17901416
64. Gilchrist M, Thorsson V, Li B, Rust AG, Korb M, et al. (2006) Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441: 173-178. PMID: 16688168
65. Hoetzenecker W, Echtenacher B, Guenova E, Hoetzenecker K, Woelbing F, et al. (2012) ROS-induced ATF3 causes susceptibility to secondary infections during sepsis-associated immunosuppression. Nat Med 18: 128-134. doi: 10.1038/nm.2557 PMID: 22179317
66. Mo C, Wang L, Zhang J, Numazawa S, Tang H, et al. (2014) The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid Redox Signal 20: 574-588. doi: 10.1089/ars.2012.5116 PMID: 23875776
67. Podechard N, Tekpli X, Catheline D, Holme JA, Rioux V, et al. (2011) Mechanisms involved in lipid accumulation and apoptosis induced by 1-nitropyrene in Hepa1c1c7 cells. Toxicol Lett 206: 289-299. doi: 10.1016/j.toxlet.2011.07.024 PMID: 21872649
68. Bourdonnay E, Morzadec C, Fardel O, Vernhet L (2009) Redox-sensitive regulation of gene expression in human primary macrophages exposed to inorganic arsenic. J Cell Biochem 107: 537-547. doi: 10.1002/jcb.22155 PMID: 19350554
69. Koike E, Hirano S, Shimojo N, Kobayashi T (2002) cDNA microarray analysis of gene expression in rat alveolar macrophages in response to organic extract of diesel exhaust particles. Toxicol Sci 67: 241-246. PMID: 12011483