Hyaluronidase modulates bleomycin-induced lung injury detected noninvasively in small rodents by radial proton MRI

Journal of Magnetic Resonance Imaging

Volumn 41, Issue 3, 2015, Pages 755-764

  Egger, Christine ^a,b   Cannet, Catherine ^a   Gérard, Christelle ^a   Dunbar, Andrew ^a   Tigani, Bruno ^a   Beckmann, Nicolau ^a  

^a NOVARTIS PHARMA AG   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Bleomycin; Fibrosis; Hyaluronic acid (hyaluronan); Lung; Magnetic resonance imaging (MRI); Ultrashort echo time (UTE)

Indexed keywords

BLEOMYCIN; BUDESONIDE; COLLAGEN; HYALURONIC ACID; HYALURONIDASE; HYALURONOGLUCOSAMINIDASE; PROTON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ANALYSIS; GLYCOSAMINOGLYCAN METABOLISM; HISTOPATHOLOGY; HYDROPHILICITY; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; FIBROSIS; LUNG; LUNG INJURY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; BLEOMYCIN; DISEASE MODELS, ANIMAL; FIBROSIS; HYALURONOGLUCOSAMINIDASE; LUNG; LUNG INJURY; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; PROTONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84923181093     PISSN: 10531807     EISSN: 15222586     Source Type: Journal    
DOI: 10.1002/jmri.24612     Document Type: Article

References (42)

1. Noble PW, Barkauskas CE, Jiang D. Pulmonary fibrosis: Patterns and perpetrators. J Clin Invest 2012;122:2756-2762.
2. Shimbori C, Gauldie J, Kolb M. Extracellular matrix microenvironment contributes actively to pulmonary fibrosis. Curr Opin Pulmon Med 2013;19:446-452.
3. Izbicki G, Segel MJ, Christensen TG, Conner MW, Breuer R. Time course of bleomycin-induced lung fibrosis. Int J Exp Pathol 2002;83:111-119.
4. Moore BB, Hogaboam CM. Murine models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008;294:L152-160.
5. Degryse AL, Tanjore H, Xu XC, et al. Repetitive intratracheal bleomycin models several features of idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2010;299:L442-452.
6. Karmouty-Quintana H, Cannet C, Zurbruegg S, et al. Bleomycin-induced lung injury assessed noninvasively and in spontaneously breathing rats by proton mri. J Magn Reson Imaging 2007;26:941-949.
7. Jacob RE, Amidan BG, Soelberg J, Minard KR. In vivo mri of altered proton signal intensity and t2 relaxation in a bleomycin model of pulmonary inflammation and fibrosis. J Magn Reson Imaging 2010;31:1091-1099.
8. Babin AL, Cannet C, Gerard C, Wyss D, Page CP, Beckmann N. Noninvasive assessment of bleomycin-induced lung injury and the effects of short-term glucocorticosteroid treatment in rats using mri. J Magn Reson Imaging 2011;33:603-614.
9. Babin AL, Cannet C, Gerard C, et al. Bleomycin-induced lung injury in mice investigated by MRI: model assessment for target analysis. Magn Reson Med 2012;67:499-509.
10. Egger C, Cannet C, Gerard C, et al. Administration of bleomycin via the oropharyngeal aspiration route leads to sustained lung fibrosis in mice and rats as quantified by UTE-MRI and histology. PLoS One 2013;8:e63432.
11. Lattanzio PJ, Marshall KW, Damyanovich AZ, Peemoeller H. Macromolecule and water magnetization exchange modeling in articular cartilage. Magn Reson Med 2000;44:840-851.
12. Clarke DL, Carruthers AM, Mustelin T, Murray LA. Matrix regulation of idiopathic pulmonary fibrosis: the role of enzymes. Fibrogen Tissue Repair 2013;6:20.
13. Negrini D, Passi A, Moriondo A. The role of proteoglycans in pulmonary edema development. Intens Care Med 2008;34:610-618.
14. Hunger J, Bernecker A, Bakker HJ, Bonn M, Richter RP. Hydration dynamics of hyaluronan and dextran. Biophys J 2012;103:L10-12.
15. Josse G, Haftek M, Gensanne D, et al. Follow up study of dermal hyaluronic acid injection by high frequency ultrasound and magnetic resonance imaging. J Dermatol Sci 2010;57:214-216.
16. Cheng G, Swaidani S, Sharma M, Lauer ME, Hascall VC, Aronica MA. Hyaluronan deposition and correlation with inflammation in a murine ovalbumin model of asthma. Matrix Biol 2011;30:126-134.
17. Wang F, Garza LA, Kang S, et al. In vivo stimulation of de novo collagen production caused by cross-linked hyaluronic acid dermal filler injections in photodamaged human skin. Arch Dermatol 2007;143:155-163.
18. Turlier V, Delalleau A, Casas C, et al. Association between collagen production and mechanical stretching in dermal extracellular matrix: in vivo effect of cross-linked hyaluronic acid filler. A randomised, placebo-controlled study. J Dermatol Sci 2013;69:187-194.
19. Bjermer L, Lundgren R, Hallgren R. Hyaluronan and type III procollagen peptide concentrations in bronchoalveolar lavage fluid in idiopathic pulmonary fibrosis. Thorax 1989;44:126-131.
20. Papakonstantinou E, Karakiulakis G. The 'sweet' and 'bitter' involvement of glycosaminoglycans in lung diseases: pharmacotherapeutic relevance. Br J Pharmacol 2009;157:1111-1127.
21. Venkatesan N, Ouzzine M, Kolb M, Netter P, Ludwig MS. Increased deposition of chondroitin/dermatan sulfate glycosaminoglycan and upregulation of beta1,3-glucuronosyltransferase I in pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2011;300:L191-203.
22. Savani RC, Hou G, Liu P, et al. A role for hyaluronan in macrophage accumulation and collagen deposition after bleomycininduced lung injury. Am J Respir Cell Mol Biol 2000;23:475-484.
23. Zaman A, Cui Z, Foley JP, et al. Expression and role of the hyaluronan receptor rhamm in inflammation after bleomycin injury. Am J Respir Cell Mol Biol 2005;33:447-454.
24. Li Y, Jiang D, Liang J, et al. Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J Exp Med 2011;208:1459-1471.
25. McKee CM, Penno MB, Cowman M, et al. Hyaluronan (ha) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest 1996;98:2403-2413.
26. Horton MR, Shapiro S, Bao C, Lowenstein CJ, Noble PW. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J Immunol 1999;162:4171-4176.
27. De Vooght V, Vanoirbeek JA, Haenen S, Verbeken E, Nemery B, Hoet PH. Oropharyngeal aspiration: an alternative route for challenging in a mouse model of chemical-induced asthma. Toxicology 2009;259:84-89.
28. Bitencourt CS, Pereira PA, Ramos SG, et al. Hyaluronidase recruits mesenchymal-like cells to the lung and ameliorates fibrosis. Fibrogen Tissue Repair 2011;4:3.
29. Ble FX, Cannet C, Zurbruegg S, et al. Activation of the lung S1P(1) receptor reduces allergen-induced plasma leakage in mice. Br J Pharmacol 2009;158:1295-1301.
30. Tigani B, Schaeublin E, Sugar R, Jackson AD, Fozard JR, Beckmann N. Pulmonary inflammation monitored noninvasively by mri in freely breathing rats. Biochem Biophys Res Commun 2002;292:216-221.
31. Selman M, Thannickal VJ, Pardo A, Zisman DA, Martinez FJ, Lynch JP 3rd. Idiopathic pulmonary fibrosis: Pathogenesis and therapeutic approaches. Drugs 2004;64:405-430.
32. Takahashi M, Togao O, Obara M, et al. Ultra-short echo time (UTE) MR imaging of the lung: comparison between normal and emphysematous lungs in mutant mice. J Magn Reson Imaging 2010;32:326-333.
33. Zurek M, Boyer L, Caramelle P, Boczkowski J, Cremillieux Y. Longitudinal and noninvasive assessment of emphysema evolution in a murine model using proton MRI. Magn Reson Med 2012;68:898-904.
34. Bianchi A, Ozier A, Ousova O, Raffard G, Cremillieux Y. Ultrashort-TE MRI longitudinal study and characterization of a chronic model of asthma in mice: inflammation and bronchial remodeling assessment. NMR Biomed 2013;26:1451-1459.
35. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative c(t) method. Nat Protocols 2008;3:1101-1108.
36. Karmouty-Quintana H, Cannet C, Sugar R, Fozard JR, Page CP, Beckmann N. Capsaicin-induced mucus secretion in rat airways assessed in vivo and non-invasively by magnetic resonance imaging. Br J Pharmacol 2007;150:1022-1030.
37. Karmouty-Quintana H, Ble FX, Cannet C, et al. In vivo pharmacological evaluation of compound 48/80-induced airways oedema by MRI. Br J Pharmacol 2008;154:1063-1072.
38. Ask K, Labiris R, Farkas L, et al. Comparison between conventional and "clinical" assessment of experimental lung fibrosis. J Transl Med 2008;6:16.
39. Shofer S, Badea C, Qi Y, Potts E, Foster WM, Johnson GA. A micro-CT analysis of murine lung recruitment in bleomycin-induced lung injury. J Appl Physiol 2008;105:669-677.
40. Jin GY, Bok SM, Han YM, et al. Effectiveness of rosiglitazone on bleomycin-induced lung fibrosis: assessed by micro-computed tomography and pathologic scores. Eur J Radiol 2012;81:1901-1906.
41. Caravan P, Yang Y, Zachariah R, et al. Molecular magnetic resonance imaging of pulmonary fibrosis in mice. Am J Respir Cell Mol Biol 2013;49:1120-1126.
42. Moeller A, Ask K, Warburton D, Gauldie J, Kolb M. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis? Int J Biochem Cell Biol 2008;40:362-382.