Ex vivo lung function measurements in precision-cut lung slices (PCLS) from chemical allergen-sensitized mice represent a suitable alternative to in vivo studies

Toxicological Sciences

Volumn 106, Issue 2, 2008, Pages 444-453

  Henjakovic, M ^a   Martin, C ^b,c   Hoymann, H G ^a   Sewald, K ^a   Ressmeyer, A R ^b,c   Dassow, C ^b,c   Pohlmann, G ^a   Krug, N ^a   Uhlig, S ^a   Braun, Armin ^a  

^a FRAUNHOFER INSTITUTE FOR TOXICOLOGY AND EXPERIMENTAL MEDICINE   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c RESEARCH CENTER BORSTEL   (Germany)

Author keywords

Bronchoconstriction; DNCB; Lung function; Methacholine; PCLS; TMA

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; CONTACT ALLERGEN; EOTAXIN; INDUSTRIAL CHEMICAL; METHACHOLINE; TRIMELLITIC ANHYDRIDE;

ALLERGENICITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BRONCHUS HYPERREACTIVITY; CONTACT ALLERGY; CONTROLLED STUDY; EOSINOPHIL COUNT; EX VIVO STUDY; FEMALE; IN VIVO STUDY; INHALATION TEST; INTERMETHOD COMPARISON; LUNG FUNCTION TEST; LUNG LAVAGE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRECISION CUT LUNG SLICE; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; TISSUE SLICE;

ALLERGENS; ANIMALS; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHOCONSTRICTION; DINITROCHLOROBENZENE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; LUNG; METHACHOLINE CHLORIDE; MICE; MICE, INBRED BALB C; PHTHALIC ANHYDRIDES; PNEUMONIA; RESPIRATORY FUNCTION TESTS;

ANIMALIA; MUS;

EID: 56649105359     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn178     Document Type: Article

References (59)

1. Arts, J. H., Bloksma, N., Leusink-Muis, T., and Kuper, C. F. (2003). Respiratory allergy and pulmonary irritation to trimellitic anhydride in Brown Norway rats. Toxicol. Appl. Pharmacol. 187, 38-49.
2. Arts, J. H., and Kuper, C. F. (2007). Animal models to test respiratory allergy of low molecular weight chemicals: A guidance. Methods 41, 61-71.
3. Arts, J. H., Kuper, C. F., Spoor, S. M., and Bloksma, N. (1998). Airway morphology and function of rats following dermal sensitization and respiratory challenge with low molecular weight chemicals. Toxicol. Appl. Pharmacol. 152, 66-76.
4. Ban, M., and Hettich, D. (2001). Relationship between IgE positive cell numbers and serum total IgE levels in mice treated with trimellitic anhydride and dinitrochlorobenzene. Toxicol. Lett. 118, 129-137.
5. Baur, X., and Czuppon, A. (1995). Diagnostic validation of specific IgE antibody concentrations, skin prick testing, and challenge tests in chemical workers with symptoms of sensitivity to different anhydrides. J. Allergy Clin. Immunol. 96, 489-494.
6. Beck, L. A., and Leung, D. Y. (2000). Allergen sensitization through the skin induces systemic allergic responses. J. Allergy Clin. Immunol. 106, S258-S263.
7. Bergner, A., and Sanderson, M. J. (2002). Acetylcholine-induced calcium signaling and contraction of airway smooth muscle cells in lung slices. J. Gen. Physiol. 119, 187-198.
8. Buckley, T. L., and Nijkamp, F. P. (1994). Mucosal exudation associated with a pulmonary delayed-type hypersensitivity reaction in the mouse. Role for the tachykinins. J. Immunol. 153, 4169-4178.
9. D'Erchia, A. M., Gissi, C., Pesole, G., Saccone, C., and Arnason, U. (1996). The guinea-pig is not a rodent. Nature 381, 597-600.
10. Dandurand, R. J., Wang, C. G., Laberge, S., Martin, J. G., and Eidelman, D. H. (1994). In vitro allergic bronchoconstriction in the brown Norway rat. Am. J. Respir. Crit. Care Med. 149, 1499-1505.
11. Dearman, R. J., Basketter, D. A., and Kimber, I. (1998). Selective induction of type 2 cytokines following topical exposure of mice to platinum salts. Food Chem. Toxicol. 36, 199-207.
12. + T lymphocyte subsets to the cytokine secretion patterns induced in mice during sensitization to contact and respiratory chemical allergens. Immunology 89, 502-510.
13. Dearman, R. J., Smith, S., Basketter, D. A., and Kimber, I. (1997). Classification of chemical allergens according to cytokine secretion profiles of murine lymph node cells. J. Appl. Toxicol. 17, 53-62.
14. Dearman, R. J., Warbrick, E. V., Humphreys, I. R., and Kimber, I. (2000). Characterization in mice of the immunological properties of five allergenic acid anhydrides. J. Appl. Toxicol. 20, 221-230.
15. Dearman, R. J., Warbrick, E. V., Skinner, R., and Kimber, I. (2002). Cytokine fingerprinting of chemical allergens: Species comparisons and statistical analyses. Food Chem. Toxicol. 40, 1881-1892.
16. Erpenbeck, V. J., Ziegert, M., Cavalet-Blanco, D., Martin, C., Baelder, R., Glaab, T., Braun, A., Steinhilber, W., Luettig, B., Uhlig, S., et al. (2006). Surfactant protein D inhibits early airway response in Aspergillus fumigatus-sensitized mice. Clin. Exp. Allergy 36 930-940.
17. Farraj, A. K., Boykin, E., Haykal-Coates, N., Gavett, S. H., Doerfler, D., and Selgrade, M. (2007). Th2 cytokines in skin draining lymph nodes and serum IgE do not predict airway hypersensitivity to intranasal isocyanate exposure in mice. Toxicol. Sci. 100, 99-108.
18. Farraj, A. K., Harkema, J. R., and Kaminski, N. E. (2006). Topical application versus intranasal instillation: A qualitative comparison of the effect of the route of sensitization on trimellitic anhydride-induced allergic rhinitis in A/J mice. Toxicol. Sci. 92, 321-328.
19. Garssen, J., Nijkamp, F. P., Van, D. H. (1991). T-cell-mediated induction of airway hyperreactivity in mice. Am. Rev. Respir. Dis. 144, 931-938.
20. Garssen, J., Nijkamp, F. P., Wagenaar, S. S., Zwart, A., Askenase, P. W., and Van Loveren, H. (1989). Regulation of delayed-type hypersensitivity-like responses in the mouse lung, determined with histological procedures: Serotonin, T-cell suppressor-inducer factor and high antigen dose tolerance regulate the magnitude of T-cell dependent inflammatory reactions. Immunology 68, 51-58.
21. Garssen, J., Van Loveren, H., Van, D., H., and Nijkamp, F. P. (1993). T cell-mediated induction of airway hyperresponsiveness and altered lung functions in mice are independent of increased vascular permeability and mononuclear cell infiltration. Am. Rev. Respir. Dis. 147, 307-313.
22. Glaab, T., Mitzner, W., Braun, A., Ernst, H., Korolewitz, R., Hohlfeld, J. M., Krug, N., and Hoymann, H. G. (2004). Repetitive measurements of pulmonary mechanics to inhaled cholinergic challenge in spontaneously breathing mice. J. Appl. Physiol. 97, 1104-1111.
23. Glaab, T., Taube, C., Braun, A., and Mitzner, W. (2007). Invasive and noninvasive methods for studying pulmonary function in mice. Respir. Res. 8, 63.
24. Glaab, T., Ziegert, M., Baelder, R., Korolewitz, R., Braun, A., Hohlfeld, J. M., Mitzner, W., Krug, N., and Hoymann, H. G. (2005). Invasive versus noninvasive measurement of allergic and cholinergic airway responsiveness in mice. Respir. Res. 6, 139.
25. Grammer, L. C., Shaughnessy, M. A., Henderson, J., Zeiss, C. R., Kavich, D. E., Collins, M. J., Pecis, K. M., and Kenamore, B. D. (1993). A clinical and immunologic study of workers with trimellitic-anhydride-induced immunologic lung disease after transfer to low exposure jobs. Am. Rev. Respir. Dis. 148, 54-57.
26. Greene, A. L., Rutherford, M. S., Regal, R. R., Flickinger, G. H., Hendrickson, J. A., Giulivi, C., Mohrman, M. E., Fraser, D. G., and Regal, J. F. (2005). Arginase activity differs with allergen in the effector phase of ovalbumin- versus trimellitic anhydride-induced asthma. Toxicol. Sci. 88, 420-433.
27. Guo, T. L., Zhang, X. L., Leffel, E. K., Peachee, V. L., Karrow, N. A., Germolec, D. R., and White, K. L., Jr. (2002). Differential stimulation of IgE production, STAT activation and cytokine and CD86 expression by 2,4-dinitrochlorobenzene and trimellitic anhydride. J. Appl. Toxicol. 22, 397-403.
28. Hayashi, M., Higashi, K., Kato, H., and Kaneko, H. (2001). Assessment of preferential Th1 or Th2 induction by low-molecular-weight compounds using a reverse transcription-polymerase chain reaction method: Comparison of two mouse strains, C57BL/6 and BALB/c. Toxicol. Appl. Pharmacol. 177, 38-45.
29. Held, H. D., Martin, C., and Uhlig, S. (1999). Characterization of airway and vascular responses in murine lungs. Br. J. Pharmacol. 126, 1191-1199.
30. Held, H. D., and Uhlig, S. (2000). Mechanisms of endotoxin-induced airway and pulmonary vascular hyperreactivity in mice. Am. J. Respir. Crit. Care Med. 162, 1547-1552.
31. Henjakovic, M., Sewald, K., Switalla, S., Kaiser, D., Muller, M., Veres, T. Z., Martin, C., Uhlig, S., Krug, N., and Braun, A. (2008). Ex vivo testing of immune responses in precision-cut lung slices. Toxicol. Appl. Pharmacol. 231, 68-76.
32. Hoymann, H. G. (2006). New developments in lung function measurements in rodents. Exp Toxicol Pathol. 57 (Suppl. 2), 5-11.
33. Karol, M. H. (1986). Respiratory effects of inhaled isocyanates. Crit. Rev. Toxicol. 16, 349-379.
34. Kimber, I., Basketter, D. A., and Roggeband, R. (2001). Chemical respiratory allergy: Classification and labelling. Toxicology 167, 159-162.
35. Kimber, I., Gerberick, G. F., Van Loveren, H., and House, R. V. (1992). Chemical allergy: Molecular mechanisms and practical applications. Fundam. Appl. Toxicol. 19, 479-483.
36. Kirschvink, N., Vincke, G., Onclinx, C., Peck, M. J., and Gustin, P. (2005). Comparison between pulmonary resistance and Penh in anaesthetised rats with tracheal diameter reduction and after carbachol inhalation. J. Pharmacol. Toxicol. Methods 51, 123-128.
37. Larsen, C. P., and Regal, J. F. (2002). Trimellitic anhydride (TMA) dust induces airway obstruction and eosinophilia in non-sensitized guinea pigs. Toxicology 178, 89-99.
38. MacLean, J. A., Sauty, A., Luster, A. D., Drazen, J. M., and De Sanctis, G. T. (1999). Antigen-induced airway hyperresponsiveness, pulmonary eosinophilia, and chemokine expression in B cell-deficient mice. Am. J. Respir. Cell Mol. Biol. 20, 379-387.
39. Mapp, C. E., Boschetto, P., Maestrelli, P., and Fabbri, L. M. (2005). Occupational asthma. Am. J. Respir. Crit. Care Med. 172, 280-305.
40. Martin, C., Uhlig, S., and Ullrich, V. (1996). Videomicroscopy of methacholine-induced contraction of individual airways in precision-cut lung slices. Eur. Respir. J. 9, 2479-2487.
41. Martin, C., Uhlig, S., and Ullrich, V. (2001). Cytokine-induced bronchoconstriction in precision-cut lung slices is dependent upon cyclooxygenase-2 and thromboxane receptor activation. Am. J. Respir. Cell Mol. Biol. 24, 139-145.
42. Neuhaus-Steinmetz, U., Glaab, T., Daser, A., Braun, A., Lommatzsch, M., Herz, U., Kips, J., Alarie, Y., and Renz, H. (2000). Sequential development of airway hyperresponsiveness and acute airway obstruction in a mouse model of allergic inflammation. Int. Arch. Allergy Immunol. 121, 57-67.
43. Path, G., Braun, A., Meents, N., Kerzel, S., Quarcoo, D., Raap, U., Hoyle, G. W., Nockher, W. A., and Renz, H. (2002). Augmentation of allergic early-phase reaction by nerve growth factor. Am. J. Respir. Crit. Care Med. 166, 818-826.
44. Pauluhn, J., Eidmann, P., Freyberger, A., Wasinska-Kempka, G., and Vohr, H. W. (2002). Respiratory hypersensitivity to trimellitic anhydride in Brown Norway rats: A comparison of endpoints. J Appl Toxicol. 22, 89-97.
45. Regal, J. F., Mohrman, M. E., and Sailstad, D. M. (2001). Trimellitic anhydride-induced eosinophilia in a mouse model of occupational asthma. Toxicol. Appl. Pharmacol. 175, 234-242.
46. Ressmeyer, A. R., Larsson, A. K., Vollmer, E., Dahlen, S. E., Uhlig, S., and Martin, C. (2006). Characterisation of guinea pig precision-cut lung slices: Comparison with human tissues. Eur. Respir. J. 28, 603-611.
47. Sailstad, D. M., Ward, M. D., Boykin, E.H., and Selgrade, M. K. (2003). A murine model for low molecular weight chemicals: Differentiation of respiratory sensitizers (TMA) from contact sensitizers (DNFB). Toxicology 194, 147-161.
48. Tarkowski, M., Vanoirbeek, J. A., Vanhooren, H. M., Vooght, V. D., Mercier, C. M., Ceuppens, J., Nemery, B., and Hoet, P. H. (2007). Immunological determinants of ventilatory changes induced in mice by dermal sensitization and respiratory challenge with toluene diisocyanate. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L207-L214.
49. Tee, R. D., Cullinan, P., Welch, J., Burge, P. S., and Newman-Taylor, A. J. (1998). Specific IgE to isocyanates: A useful diagnostic role in occupational asthma. J. Allergy Clin. Immunol. 101, 709-715.
50. Valstar, D. L., Schijf, M. A., Stelekati, E., Nijkamp, F. P., Bloksma, N., and Henricks, P. A. (2006). Trimellitic anhydride-conjugated serum albumin activates rat alveolar macrophages in vitro. J. Occup.Med. Toxicol. 1, 13.
51. Vandebriel, R. J., De Jong, W. H., Hendriks, J. J., and Van Loveren, H. (2003). Impact of exposure duration by low molecular weight compounds on interferon-gamma and interleukin-4 mRNA expression and production in the draining lymph nodes of mice. Toxicology 188, 1-13.
52. Vandebriel, R. J., De Jong, W. H., Spiekstra, S. W., Van Dijk, M., Fluitman, A., Garssen, J., and Van Loveren, H. (2000). Assessment of preferential T-helper 1 or T-helper 2 induction by low molecular weight compounds using the local lymph node assay in conjunction with RT-PCR and ELISA for interferon-gamma and interleukin-4. Toxicol. Appl. Pharmacol. 162, 77-85.
53. Vanoirbeek, J. A., Tarkowski, M., Vanhooren, H. M., De Vooght, V., Nemery, B., and Hoet, P. H. (2006). Validation of a mouse model of chemical-induced asthma using trimellitic anhydride, a respiratory sensitizer, and dinitrochlorobenzene, a dermal sensitizer. J. Allergy Clin. Immunol. 117, 1090-1097.
54. Wohlsen, A., Martin, C., Vollmer, E., Branscheid, D., Magnussen, H., Becker, W. M., Lepp, U., and Uhlig, S. (2003). The early allergic response in small airways of human precision-cut lung slices. Eur. Respir. J. 21, 1024-1032.
55. Wohlsen, A., Uhlig, S., and Martin, C. (2001). Immediate allergic response in small airways. Am. J. Respir. Crit. Care Med. 163 1462-1469.
56. Zeiss, C. R., Patterson, R., Pruzansky, J. J., Miller, M. M., Rosenberg, M., and Levitz, D. (1977). Trimellitic anhydride-induced airway syndromes: Clinical and immunologic studies. J. Allergy Clin. Immunol. 60, 96-103.
57. Zhang, X. D., Andrew, M. E., Hubbs, A. F., and Siegel, P. D. (2006). Airway responses in Brown Norway rats following inhalation sensitization and challenge with trimellitic anhydride. Toxicol. Sci. 94, 322-329.
58. Zhang, X. D., Fedan, J. S., Lewis, D. M., and Siegel, P. D. (2004). Asthmalike biphasic airway responses in Brown Norway rats sensitized by dermal exposure to dry trimellitic anhydride powder. J. Allergy. Clin. Immunol. 113, 320-326.
59. Zosky, G. R., Larcombe, A. N., White, O. J., Burchell, J. T., Janosi, T. Z., Hantos, Z., Holt, P. G., Sly, P. D., and Turner, D. J. (2008). Ovalbumin-sensitized mice are good models for airway hyperresponsiveness but not acute physiological responses to allergen inhalation. Clin. Exp. Allergy 38, 829-838.