Biokinetics of nanoparticles and susceptibility to particulate exposure in a murine model of cystic fibrosis

Particle and Fibre Toxicology

Volumn 11, Issue 1, 2014, Pages

  Geiser, Marianne ^a   Stoeger, Tobias ^b   Casaulta, Marco ^a   Chen, Shanze ^b   Semmler Behnke, Manuela ^b   Bolle, Ines ^b   Takenaka, Shinji ^b   Kreyling, Wolfgang G ^b   Schulz, Holger ^b  

^a UNIVERSITY OF BERN   (Switzerland)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Aerosol; Biokinetics; Cystic fibrosis; Energy filtering transmission electron microscopy; Inflammation; Inhalation; Iridium; Lung function; Nanoparticles; Titanium dioxide; Ultrafine particles

Indexed keywords

CARBON; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GRANULOCYTE COLONY STIMULATING FACTOR; IRIDIUM; NANOPARTICLE; TITANIUM DIOXIDE;

AIR POLLUTION; AIRWAY RESISTANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR GENE; FEMALE; GENOTYPE; LUNG ALVEOLUS EPITHELIUM; LUNG CLEARANCE; LUNG COMPLIANCE; LUNG LAVAGE; LUNG STRUCTURE; MALE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; TISSUE DISTRIBUTION; TRANSMISSION ELECTRON MICROSCOPY; TRANSPORT KINETICS; WILD TYPE;

AIR POLLUTANTS; AIR POLLUTION; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOHISTOCHEMISTRY; INHALATION EXPOSURE; IRIDIUM; IRIDIUM RADIOISOTOPES; LUNG; MALE; MICE; MICE, INBRED CFTR; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; NANOPARTICLES; PNEUMONIA; RESPIRATORY FUNCTION TESTS; TITANIUM;

EID: 84899959556     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-11-19     Document Type: Article

References (50)

1. WHO Burden of disease from air pollution for 2012 2014, Geneva: World Health Organization 2014, http://www.who.int/mediacentre/news/releases/2014/air-pollution/en/, WHO.
2. Anderson JO, Thundiyil JG, Stolbach A. Clearing the air: a review of the effects of particulate matter air pollution on human health. J Med Toxicol 2012, 8(2):166-175. 10.1007/s13181-011-0203-1, 3550231, 22194192.
3. Brook RD, Rajagopalan S, Pope CA, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC, Whitsel L, Kaufman JD. American Heart Association Council on Epidemiology and Prevention, Council on the Kidney in Cardiovascular Disease, and Council on Nutrition, Physical Activity and Metabolism: Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation 2010, 121(21):2331-2378. 10.1161/CIR.0b013e3181dbece1, 20458016.
4. Rückerl R, Schneider A, Breitner S, Cyrys J, Peters A. Health effects of particulate air pollution: a review of epidemiological evidence. Inhal Toxicol 2011, 23(10):555-592. 10.3109/08958378.2011.593587, 21864219.
5. Kelly FJ, Fussell JC. Air pollution and airway disease. Clin Exp Allergy 2011, 41(8):1059-1071. 10.1111/j.1365-2222.2011.03776.x, 21623970.
6. Bear CE, Li C, Kartner N, Bridges RJ, Jensen TJ, Ramjeesingh M, Riordan JR. Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR). Cell 1992, 68:809-818. 10.1016/0092-8674(92)90155-6, 1371239.
7. Donaldson SH, Boucher RC. Update on pathogenesis of cystic fibrosis lung disease. Curr Opin Pulm Med 2003, 9:486-491. 10.1097/00063198-200311000-00007, 14534400.
8. Hauser AR, Jain M, Bar-Meir M, McColley SA. Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 2011, 24(1):29-70. 10.1128/CMR.00036-10, 3021203, 21233507.
9. Khan TZ, Wagener JS, Bost T, Martinez J, Accurso FJ, Riches DW. Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med 1995, 151:1075-1082.
10. Boyle MP. Strategies for identifying modifier genes in cystic fibrosis. Proc Am Thorac Soc 2007, 4(1):52-57. 10.1513/pats.200605-129JG, 2647615, 17202292.
11. Hamosh A, Corey M. Correlation between genotype and phenotype in patients with cystic fibrosis The Cystic Fibrosis Genotype-Phenotype Consortium. N Engl J Med 1993, 329:1308-1313.
12. Goss CH, Newsom SA, Schildcrout JS, Sheppard L, Kaufman JD. Effect of ambient air pollution on pulmonary exacerbations and lung function in cystic fibrosis. Am J Respir Crit Care Med 2004, 169:816-821. 10.1164/rccm.200306-779OC, 14718248.
13. Brown JS, Bennett WD. Deposition of coarse particles in cystic fibrosis: model predictions versus experimental results. J Aerosol Med 2004, 17(3):239-248. 10.1089/jam.2004.17.239, 15625816.
14. Geiser M. Update on macrophage clearance of inhaled micro- and nanoparticles. J Aerosol Med Pulm Drug Deliv 2010, 23(4):207-217. 10.1089/jamp.2009.0797, 20109124.
15. Randell SH, Boucher RC. Effective mucus clearance is essential for respiratory health. Am J Respir Cell Mol Biol 2006, 35:20-28. 10.1165/rcmb.2006-0082SF, 2658694, 16528010.
16. Kreyling WG, Tuch T, Peters A, Pitz M, Heinrich J, Stolzel M, Cyrys J, Heyder J, Wichmann HE. Diverging long-term trends in ambient urban particle mass and number concentrations associated with emission changes caused by the German unification. Atmos Environ 2003, 37:3841-3848.
17. Landy MK, Roberts MJ, Thomas SR. The wrong questions and why. The Environmental Protection Agency: asking the wrong questions 1990, New York, NY: Oxford University Press.
18. Landy MK, Roberts MJ, Thomas SR. Good questions. The Environmental Protection Agency: asking the wrong questions 1990, New York, NY: Oxford University Press.
19. Möller W, Felten K, Sommerer K, Scheuch G, Meyer G, Meyer P, Häussinger K, Kreyling WG. Deposition, retention and translocation of ultrafine particles from the central airways and lung periphery. Am J Respir Crit Care Med 2008, 177:426-432. 10.1164/rccm.200602-301OC, 17932382.
20. Geiser M, Quaile O, Wenk A, Wigge C, Eigeldinger-Berthou S, Hirn S, Schäffler M, Schleh C, Möller W, Mall MA, Kreyling WG. Cellular uptake and localization of inhaled gold nanoparticles in lungs of mice with chronic obstructive pulmonary disease. Particle Fibre Toxicol 2013, 10:19.
21. Dorin JR, Dickinson P, Alton EW, Smith SN, Geddes DM, Stevenson BJ, Kimber WL, Fleming S, Clarke AR, Hooper ML, Andersen L, Beddington RSP, Porteous DJ. Cystic fibrosis in the mouse by targeted insertional mutagenesis. Nature 1992, 359:211-215. 10.1038/359211a0, 1382232.
22. Geiser M, Zimmermann B, Baumann M, Cruz-Orive LM. Does lack of Cftr gene lead to developmental abnormalities in the lung?. Exp Lung Res 2000, 26:551-564. 10.1080/019021400750048090, 11076312.
23. Geiser M, Bastian S. Surface-lining layer of airways in cystic fibrosis mice. Am J Physiol Lung Cell Mol Physiol 2003, 285:L1277-L1285.
24. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008, 9(8):639-649. 10.1038/nrm2447, 2851551, 18612320.
25. André E, Stoeger T, Takenaka S, Bahnweg M, Ritter B, Karg E, Lentner B, Reinhard C, Schulz H, Wjst M. Inhalation of ultrafine carbon particles triggers biphasic pro-inflammatory response in the mouse lung. Eur Respir J 2006, 28(2):275-285. 10.1183/09031936.06.00071205, 16641123.
26. Geiser M, Rothen-Rutishauser B, Kapp N, Schürch S, Kreyling W, Schulz H, Semmler M, Im Hof V, Heyder J, Gehr P. Ultrafine particles cross cellular membranes by non-phagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 2005, 113:1555-1560. 10.1289/ehp.8006, 1310918, 16263511.
27. Mühlfeld C, Gehr P, Rothen-Rutishauser B. Translocation and cellular entering mechanisms of nanoparticles in the respiratory tract. Swiss Med Wkly 2008, 138:387-391.
28. Van de Weert-van Leeuwen PB, Van Meegen MA, Speirs JJ, Pals DJ, Rooijakkers SH, Van der Ent CK, Terheggen-Lagro SW, Arets HG, Beekman JM. Optimal complement-mediated phagocytosis of Pseudomonas aeruginosa by monocytes is cystic fibrosis transmembrane conductance regulator-dependent. Am J Respir Cell Mol Biol 2013, 49(3):463-470. 10.1165/rcmb.2012-0502OC, 23617438.
29. Rimai DS, Quesnel DJ, Busnaia AA. The adhesion of dry particles in the nanometer to micrometer-size range. Colloid Surface Physicochem Eng Aspect 2000, 165:3-10.
30. Nadel JA, Conrad DJ, Ueki IF, Schuster A, Sigal E. Immunocytochemical localization of arachidonate 15-lipoxygenase in erythrocytes, leukocytes, and airway cells. J Clin Invest 1991, 87(4):1139-1145. 10.1172/JCI115110, 295116, 2010530.
31. Profita M, Sala A, Riccobono L, Pace E, Paternò A, Zarini S, Siena L, Mirabella A, Bonsignore G, Vignola AM. 15(S)-HETE modulates LTB (4) production and neutrophil chemotaxis in chronic bronchitis. Am J Physiol Cell Physiol 2000, 279(4):C1249-C1258.
32. Harmon GS, Dumlao DS, Ng DT, Barrett KE, Dennis EA, Dong H, Glass CK. Pharmacological correction of a defect in PPAR-gamma signaling ameliorates disease severity in Cftr-deficient mice. Nat Med 2010, 16(3):313-318. 10.1038/nm.2101, 2834836, 20154695.
33. Dorin JR, Stevenson BJ, Fleming S, Alton EW, Dickinson P, Porteous DJ. Long term survival of the exon 10 insertional cystic fibrosis mutant mouse is a consequence of low level residual wild type Cftr gene expression. Mamm Genome 1994, 5:465-472. 10.1007/BF00369314, 7949729.
34. Davidson DJ, Dorin JR, McLachlan G, Ranaldi V, Lamb D, Doherty C, Govan J, Porteous DJ. Lung disease in the cystic fibrosis mouse exposed to bacterial pathogens. Nat Genet 1995, 9:351-357. 10.1038/ng0495-351, 7540910.
35. Kreyling WG, Semmler M, Erbe F, Mayer P, Takenaka S, Schulz H, Oberdörster G, Ziesenis A. Translocation of ultrafine insoluble iridium particles from lung epithelium to extrapulmonary organs is size dependent but very low. J Toxicol Environ Health-Part A 2002, 65:1513-1530.
36. Szymczak W, Menzel N, Kreyling WG, Wittmaack K. TOF-SIMS characterisation of spark-generated nanoparticles made from pairs of Ir-Ir and Ir-C electrodes. Internat J Mass Spectrom 2006, 254:70-84.
37. Kapp N, Kreyling W, Schulz H, Im Hof V, Semmler M, Gehr P, Geiser M. Identification of inhaled ultrafine titanium oxide particles by analytical electron microscopy in rat lungs. Microsc Res Techn 2004, 63:298-305.
38. Stoeger T, Reinhard C, Takenaka S, Schroeppel A, Karg E, Ritter B, Heyder J, Schulz H. Instillation of six different ultrafine carbon particles indicates a surface area threshold dose for acute lung inflammation in mice. Environ Health Perspect 2006, 114(3):328-333. 1392224, 16507453.
39. Kreyling WG, Biswas P, Messing ME, Gibson N, Geiser M, Wenk A, Sahu M, Deppert K, Cydzik I, Wigge C, Schmid O, Semmler-Behnke M. Generation and characterization of stable, highly concentrated titanium dioxide nanoparticle aerosols for rodent inhalation studies. J Nanopart Res 2010, 13:511-524.
40. Stoeger T, Takenaka S, Frankenberger B, Ritter B, Karg E, Maier K, Schulz H, Schmid O. Deducing in vivo toxicity of combustion-derived nanoparticles from a cell-free oxidative potency assay and metabolic activation of organic compounds. Environ Health Perspect 2009, 117(1):54-60. 2627865, 19165387.
41. Matuschek G, Karg E, Schröppel A, Schulz H, Schmid O. Chemical investigation of eight different types of carbonaceous particles using thermoanalytical techniques. Environ Sci Technol 2007, 41:8406-8411. 10.1021/es062660v, 18200871.
42. Scherle W. A simple method for volumetry of organs in quantitative stereology. Mikroskopie 1970, 26:57-60.
43. Im Hof V, Scheuch G, Geiser M, Gebhard J, Gehr P, Heyder J. Techniques for the determination of particle deposition in lungs of hamsters. J Aerosol Med 1989, 2:247-259.
44. Reinhard C, Eder G, Fuchs H, Ziesenis A, Heyder J, Schulz H. Inbred strain variation in lung function. Mamm Genome 2002, 13:429-437. 10.1007/s00335-002-3005-6, 12226708.
45. Reinhard C, Meyer B, Fuchs H, Stoeger T, Eder G, Ruschendorf F, Heyder J, Nurnberg P, de Angelis MH, Schulz H. Genomewide linkage analysis identifies novel genetic loci for lung function in mice. Am J Respir Crit Care Med 2005, 171:880-888. 10.1164/rccm.200409-1204OC, 15640362.
46. Semmler-Behnke M, Kreyling WG, Schulz H, Takenaka S, Butler JP, Henry FS, Tsuda A. Nanoparticle delivery in infant lungs. Proc Natl Acad Sci U S A 2012, 109(13):5092-5097. 10.1073/pnas.1119339109, 3323983, 22411799.
47. Roth C, Ferron GA, Karg E, Lentner B, Schumann G, Takenaka S, Heyder J. Generation of ultrafine particles by spark discharging. Aerosol Sci Techn 2004, 38:228-235.
48. Su DS, Jentoft RE, Muller JO, Rothe D, Jacob E, Simpson CD, Tomović T, Müllen K, Messerer A, Pöschl U, Niessner R, Schlögl R. Microstructure and oxidation behaviour of Euro IV diesel engine soot: a comparative study with synthetic model soot substances. Catal Today 2004, 90:127-132.
49. Götz AA, Vidal-Puig A, Rödel HG, de Angelis MH, Stoeger T. Carbon-nanoparticle-triggered acute lung inflammation and its resolution are not altered in PPARγ-defective (P465L) mice. Part Fibre Toxicol 2011, 8:28. 10.1186/1743-8977-8-28, 3197489, 21933390.
50. Beck-Speier I, Dayal N, Karg E, Maier KL, Schumann G, Schulz H, Semmler M, Takenaka S, Stettmaier K, Bors W, Ghio A, Samet JM, Heyder J. Oxidative stress and lipid mediators induced in alveolar macrophages by ultrafine particles. Free Radic Biol Med 2005, 38:1080-1092. 10.1016/j.freeradbiomed.2005.01.004, 15780766.