Indoor Pollutant Hexabromocyclododecane Has a Modest Immunomodulatory Effect on House Dust Mite Induced Allergic Asthma in Mice

Environmental Science and Technology

Volumn 50, Issue 1, 2016, Pages 405-411

  Canbaz, Derya ^a   Logiantara, Adrian ^a   Hamers, Timo ^b   Van Ree, Ronald ^a   Van Rijt, Leonie S ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CONSUMER PRODUCTS; DISEASES; DUST; HOUSES; MAMMALS; POLLUTION;

AIRWAY INFLAMMATION; ALLERGIC ASTHMA; CYTOKINE PRODUCTION; DENDRITIC CELLS; HEXABROMOCYCLODODECANES; IMMUNE-MODULATING EFFECTS; IMMUNOMODULATORY EFFECTS; INDOOR POLLUTANTS;

AIR POLLUTION;

HEXABROMOCYCLODODECANE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; AIR POLLUTANT; ALLERGEN; BROMINATED HYDROCARBON; HOUSE DUST ALLERGEN; IMMUNOLOGIC FACTOR;

ALLERGY; ASTHMA; ATMOSPHERIC POLLUTION; IMMUNE RESPONSE; INDOOR AIR; MITE; PERSISTENT ORGANIC POLLUTANT; RISK FACTOR;

ADOPTIVE TRANSFER; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DERMATOPHAGOIDES; ENVIRONMENTAL EXPOSURE; FEMALE; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; INDOOR AIR POLLUTION; INFLAMMATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROVOCATION TEST; AIR POLLUTANT; ANIMAL; ASTHMA; CELLULAR IMMUNITY; DRUG EFFECTS; IMMUNOLOGY; PHARMACOLOGY;

MUS; PYROGLYPHIDAE;

AIR POLLUTANTS; ALLERGENS; ANIMALS; ANTIGENS, DERMATOPHAGOIDES; ASTHMA; HYDROCARBONS, BROMINATED; IMMUNITY, CELLULAR; IMMUNOLOGIC FACTORS; MICE;

EID: 84953439998     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b05348     Document Type: Article

References (43)

1. Zollner, I. K.; Weiland, S. K.; Piechotowski, I.; Gabrio, T.; von Mutius, E.; Link, B.; Pfaff, G.; Kouros, B.; Wuthe, J. No increase in the prevalence of asthma, allergies, and atopic sensitisation among children in Germany: 1992-2001 Thorax 2005, 60 (7) 545-548 10.1136/thx.2004.029561
2. Ronchetti, R.; Villa, M. P.; Barreto, M.; Rota, R.; Pagani, J.; Martella, S.; Falasca, C.; Paggi, B.; Guglielmi, F.; Ciofetta, G. Is the increase in childhood asthma coming to an end? Findings from three surveys of schoolchildren in Rome, Italy Eur. Respir. J. 2001, 17 (5) 881-6 10.1183/09031936.01.17508810
3. Hansen, E. F.; Rappeport, Y.; Vestbo, J.; Lange, P. Increase in prevalence and severity of asthma in young adults in Copenhagen Thorax 2000, 55 (10) 833-6 10.1136/thorax.55.10.833
4. Crinnion, W. J. Do Environmental Toxicants Contribute to Allergy and Asthma? Altern. Med. Rev. 2012, 17 (1) 6-18
5. Jaakkola, J. J.; Knight, T. L. The role of exposure to phthalates from polyvinyl chloride products in the development of asthma and allergies: a systematic review and meta-analysis Environ. Health Perspect 2008, 116 (7) 845-53 10.1289/ehp.10846
6. Frederiksen, M.; Vorkamp, K.; Thomsen, M.; Knudsen, L. E. Human internal and external exposure to PBDEs-A review of levels and sources Int. J. Hyg. Environ. Health 2009, 212 (2) 109-34 10.1016/j.ijheh.2008.04.005
7. Harrad, S.; de Wit, C. A.; Abdallah, M. A.; Bergh, C.; Bjorklund, J. A.; Covaci, A.; Darnerud, P. O.; de Boer, J.; Diamond, M.; Huber, S.; Leonards, P.; Mandalakis, M.; Ostman, C.; Haug, L. S.; Thomsen, C.; Webster, T. F. Indoor contamination with hexabromocyclododecanes, polybrominated diphenyl ethers, and perfluoroalkyl compounds: an important exposure pathway for people? Environ. Sci. Technol. 2010, 44 (9) 3221-31 10.1021/es903476t
8. Gallucci, S.; Matzinger, P. Danger signals: SOS to the immune system Curr. Opin. Immunol. 2001, 13 (1) 114-9 10.1016/S0952-7915(00)00191-6
9. Lambrecht, B. N.; Hammad, H. Opinion-Taking our breath away: dendritic cells in the pathogenesis of asthma Nat. Rev. Immunol. 2003, 3 (12) 994-1003 10.1038/nri1249
10. Lambrecht, B. N.; Hammad, H. Biology of Lung Dendritic Cells at the Origin of Asthma Immunity 2009, 31 (3) 412-424 10.1016/j.immuni.2009.08.008
11. Wang, Y. H.; Wills-Karp, M. The potential role of interleukin-17 in severe asthma Curr. Allergy Asthma Rep. 2011, 11 (5) 388-94 10.1007/s11882-011-0210-y
12. Cosmi, L.; Liotta, F.; Maggi, E.; Romagnani, S.; Annunziato, F. Th17 cells: new players in asthma pathogenesis Allergy 2011, 66 (8) 989-98 10.1111/j.1398-9995.2011.02576.x
13. Newcomb, D. C.; Peebles, R. S., Jr. Th17-mediated inflammation in asthma Curr. Opin. Immunol. 2013, 25 (6) 755-60 10.1016/j.coi.2013.08.002
14. Maes, T.; Provoost, S.; Lanckacker, E. A.; Cataldo, D. D.; Vanoirbeek, J. A.; Nemery, B.; Tournoy, K. G.; Joos, G. F. Mouse models to unravel the role of inhaled pollutants on allergic sensitization and airway inflammation Respir Res. 2010, 11, 7 10.1186/1465-9921-11-7
15. Brandt, E. B.; Kovacic, M. B.; Lee, G. B.; Gibson, A. M.; Acciani, T. H.; Le Cras, T. D.; Ryan, P. H.; Budelsky, A. L.; Khurana Hershey, G. K. Diesel exhaust particle induction of IL-17A contributes to severe asthma J. Allergy Clin. Immunol. 2013, 132 (5) 1194-1204.e2 10.1016/j.jaci.2013.06.048
16. Law, R. J.; Allchin, C. R.; de Boer, J.; Covaci, A.; Herzke, D.; Lepom, P.; Morris, S.; Tronczynski, J.; de Wit, C. A. Levels and trends of brominated flame retardants in the European environment Chemosphere 2006, 64 (2) 187-208 10.1016/j.chemosphere.2005.12.007
17. Roosens, L.; Abdallah, M. A.; Harrad, S.; Neels, H.; Covaci, A. Exposure to hexabromocyclododecanes (HBCDs) via dust ingestion, but not diet, correlates with concentrations in human serum: preliminary results Environ. Health Perspect 2009, 117 (11) 1707-12 10.1289/ehp.0900869
18. Abdallah, M. A.; Harrad, S. Tetrabromobisphenol-A, hexabromocyclododecane and its degradation products in UK human milk: relationship to external exposure Environ. Int. 2011, 37 (2) 443-8 10.1016/j.envint.2010.11.008
19. Sjodin, A.; Patterson, D. G., Jr.; Bergman, A. A review on human exposure to brominated flame retardants - particularly polybrominated diphenyl ethers Environ. Int. 2003, 29 (6) 829-39 10.1016/S0160-4120(03)00108-9
20. van der Ven, L. T.; Verhoef, A.; van de Kuil, T.; Slob, W.; Leonards, P. E.; Visser, T. J.; Hamers, T.; Herlin, M.; Hakansson, H.; Olausson, H.; Piersma, A. H.; Vos, J. G. A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats Toxicol. Sci. 2006, 94 (2) 281-92 10.1093/toxsci/kfl113
21. van der Ven, L. T.; van de Kuil, T.; Leonards, P. E.; Slob, W.; Lilienthal, H.; Litens, S.; Herlin, M.; Hakansson, H.; Canton, R. F.; van den Berg, M.; Visser, T. J.; van Loveren, H.; Vos, J. G.; Piersma, A. H. Endocrine effects of hexabromocyclododecane (HBCD) in a one-generation reproduction study in Wistar rats Toxicol. Lett. 2009, 185 (1) 51-62 10.1016/j.toxlet.2008.12.003
22. Saegusa, Y.; Fujimoto, H.; Woo, G. H.; Ohishi, T.; Wang, L.; Mitsumori, K.; Nishikawa, A.; Shibutani, M. Transient aberration of neuronal development in the hippocampal dentate gyrus after developmental exposure to brominated flame retardants in rats Arch. Toxicol. 2012, 86 (9) 1431-42 10.1007/s00204-012-0824-4
23. Yanagisawa, R.; Koike, E.; Win-Shwe, T. T.; Yamamoto, M.; Takano, H. Impaired lipid and glucose homeostasis in hexabromocyclododecane-exposed mice fed a high-fat diet Environ. Health Perspect 2014, 122 (3) 277-83 10.1289/ehp.1307421
24. Darnerud, P. O. Toxic effects of brominated flame retardants in man and in wildlife Environ. Int. 2003, 29 (6) 841-53 10.1016/S0160-4120(03)00107-7
25. Koike, E.; Yanagisawa, R.; Takigami, H.; Takano, H. Brominated flame retardants stimulate mouse immune cells in vitro J. Appl. Toxicol. 2013, 33 (12) 1451-9 10.1002/jat.2809
26. Hachisuka, A.; Nakamura, R.; Sato, Y.; Nakamura, R.; Shibutani, M.; Teshima, R. Effects of perinatal exposure to the brominated flame-retardant hexabromocyclododecane (HBCD) on the developing immune system in rats Kokuritsu Iyakuhin Shokuhin Eisei Kenkyujo Hokoku (Bulletin of National Institute of Health Sciences) 2010, 128, 58-64
27. An, J.; Zou, W.; Chen, C.; Zhong, F. Y.; Yu, Q. Z.; Wang, Q. J. The cytological effects of HBCDs on human hepatocyte L02 and the potential molecular mechanism J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2013, 48 (11) 1333-42 10.1080/10934529.2013.781875
28. Zou, W.; Chen, C.; Zhong, Y.; An, J.; Zhang, X.; Yu, Y.; Yu, Z.; Fu, J. PI3K/Akt pathway mediates Nrf2/ARE activation in human L02 hepatocytes exposed to low-concentration HBCDs Environ. Sci. Technol. 2013, 47 (21) 12434-40 10.1021/es401791s
29. Sheng, K. C.; Pietersz, G. A.; Tang, C. K.; Ramsland, P. A.; Apostolopoulos, V. Reactive oxygen species level defines two functionally distinctive stages of inflammatory dendritic cell development from mouse bone marrow J. Immunol. 2010, 184 (6) 2863-72 10.4049/jimmunol.0903458
30. Batal, I.; Azzi, J.; Mounayar, M.; Abdoli, R.; Moore, R.; Lee, J. Y.; Rosetti, F.; Wang, C.; Fiorina, P.; Sackstein, R.; Ichimura, T.; Abdi, R. The mechanisms of up-regulation of dendritic cell activity by oxidative stress J. Leukocyte Biol. 2014, 96 (2) 283-93 10.1189/jlb.3A0113-033RR
31. van Rijt, L. S.; Prins, J. B.; Leenen, P. J.; Thielemans, K.; de Vries, V. C.; Hoogsteden, H. C.; Lambrecht, B. N. Allergen-induced accumulation of airway dendritic cells is supported by an increase in CD31(hi)Ly-6C(neg) bone marrow precursors in a mouse model of asthma Blood 2002, 100 (10) 3663-71 10.1182/blood-2002-03-0673
32. Ryter, S. W.; Tyrrell, R. M. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties Free Radical Biol. Med. 2000, 28 (2) 289-309 10.1016/S0891-5849(99)00223-3
33. Silva, J. S.; Andrade, A. C.; Santana, C. C.; Santos, L. Q.; de Oliveira, C. I.; Veras, P. S.; Vassallo, J.; dos-Santos, W. L. Low CXCL13 expression, splenic lymphoid tissue atrophy and germinal center disruption in severe canine visceral leishmaniasis PLoS One 2012, 7 (1) e29103 10.1371/journal.pone.0029103
34. Hamelmann, E.; Schwarze, J.; Takeda, K.; Oshiba, A.; Larsen, G. L.; Irvin, C. G.; Gelfand, E. W. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography Am. J. Respir. Crit. Care Med. 1997, 156 (3) 766-75 10.1164/ajrccm.156.3.9606031
35. van Rijt, L. S.; Kuipers, H.; Vos, N.; Hijdra, D.; Hoogsteden, H. C.; Lambrecht, B. N. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma J. Immunol. Methods 2004, 288 (1-2) 111-21 10.1016/j.jim.2004.03.004
36. van Rijt, L. S.; Jung, S.; KleinJan, A.; Vos, N.; Willart, M.; Duez, C.; Hoogsteden, H. C.; Lambrecht, B. N. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma J. Exp. Med. 2005, 201 (6) 981-91 10.1084/jem.20042311
37. Canbaz, D.; Utsch, L.; Logiantara, A.; van Ree, R.; van Rijt, L. S. IL-33 promotes the induction of immunoglobulin production after inhalation of house dust mite extract in mice Allergy 2015, 70 (5) 522-32 10.1111/all.12594
38. Kimura, A.; Kishimoto, T. IL-6: regulator of Treg/Th17 balance Eur. J. Immunol. 2010, 40 (7) 1830-5 10.1002/eji.201040391
39. Peters, M.; Dudziak, K.; Stiehm, M.; Bufe, A. T-cell polarization depends on concentration of the danger signal used to activate dendritic cells Immunol. Cell Biol. 2010, 88 (5) 537-44 10.1038/icb.2010.3
40. Zhou, L.; Ivanov, II; Spolski, R.; Min, R.; Shenderov, K.; Egawa, T.; Levy, D. E.; Leonard, W. J.; Littman, D. R. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways Nat. Immunol. 2007, 8 (9) 967-74 10.1038/ni1488
41. Hammad, H.; Chieppa, M.; Perros, F.; Willart, M. A.; Germain, R. N.; Lambrecht, B. N. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells Nat. Med. 2009, 15 (4) 410-6 10.1038/nm.1946
42. Kudo, M.; Melton, A. C.; Chen, C.; Engler, M. B.; Huang, K. E.; Ren, X.; Wang, Y.; Bernstein, X.; Li, J. T.; Atabai, K.; Huang, X.; Sheppard, D. IL-17A produced by alphabeta T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction Nat. Med. 2012, 18 (4) 547-54 10.1038/nm.2684
43. Abdallah, M. A.; Harrad, S.; Covaci, A. Hexabromocyclododecanes and tetrabromobisphenol-A in indoor air and dust in Birmingham, U.K: implications for human exposure Environ. Sci. Technol. 2008, 42 (18) 6855-61 10.1021/es801110a