Effects of nintedanib on the microvascular architecture in a lung fibrosis model

Angiogenesis

Volumn 20, Issue 3, 2017, Pages 359-372

  Ackermann, Maximilian ^a   Kim, Yong Ook ^a   Wagner, Willi L ^a   Schuppan, Detlef ^a,b   Valenzuela, Cristian D ^c   Mentzer, Steven J ^c   Kreuz, Sebastian ^d   Stiller, Detlef ^d   Wollin, Lutz ^d   Konerding, Moritz A ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

Angiogenesis inhibitors; Idiopathic pulmonary fibrosis; Intussusceptive angiogenesis; Microvascular corrosion casting; Synchrotron radiation tomographic microscopy

Indexed keywords

BLEOMYCIN; COLLAGEN; GELATINASE A; HYDROXYETHYLCELLULOSE; NINTEDANIB; PROCOLLAGEN; PROCOLLAGEN ALPHA1; RESIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; INDOLE DERIVATIVE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; FIBROSING ALVEOLITIS; FORCED VITAL CAPACITY; HISTOLOGY; INFLAMMATORY CELL; LUNG ALVEOLUS; LUNG BLOOD VESSEL; LUNG COMPLIANCE; LUNG FUNCTION; LUNG LAVAGE; LUNG VOLUME; MICRO-COMPUTED TOMOGRAPHY; MICROSCOPY; MICROVASCULATURE; MORPHOMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SYNCHROTRON RADIATION; TOMOGRAPHY; ANIMAL; C57BL MOUSE; COMPLICATION; DIAGNOSTIC IMAGING; DISEASE MODEL; DRUG EFFECTS; LUNG FUNCTION TEST; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PNEUMONIA; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

ANIMALS; BLEOMYCIN; CELL PROLIFERATION; COLLAGEN; DISEASE MODELS, ANIMAL; IDIOPATHIC PULMONARY FIBROSIS; IMAGING, THREE-DIMENSIONAL; INDOLES; MICE, INBRED C57BL; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; PNEUMONIA; PULMONARY ALVEOLI; RESPIRATORY FUNCTION TESTS; X-RAY MICROTOMOGRAPHY;

EID: 85014782011     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-017-9543-z     Document Type: Article

References (37)

1. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, Lynch DA, Ryu JH, Swigris JJ, Wells AU, Ancochea J, Bouros D, Carvalho C, Costabel U, Ebina M, Hansell DM, Johkoh T, Kim DS, King TE, Kondoh Y, Myers J, Muller NL, Nicholson AG, Richeldi L, Selman M, Dudden RF, Griss BS, Protzko SL, Schunemann HJ (2011) An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 183:788–824
2. King TE Jr, Pardo A, Selman M (2011) Idiopathic pulmonary fibrosis. Lancet 378:1949–1961
3. Bonner JC (2004) Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev 15:255–273
4. Inoue Y, King TE Jr, Barker E, Daniloff E, Newman LS (2002) Basic fibroblast growth factor and its receptors in idiopathic pulmonary fibrosis and lymphangioleiomyomatosis. Am J Respir Crit Care Med 166:765–773
5. Khalil N, O’Connor RN, Unruh HW, Warren PW, Flanders KC, Kemp A, Bereznay OH, Greenberg AH (1991) Increased production and immunohistochemical localization of transforming growth factor-beta in idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 5:155–162
6. Hilberg F, Roth GJ, Krssak M, Kautschitsch S, Sommergruber W, Tontsch-Grunt U, Garin-Chesa P, Bader G, Zoephel A, Quant J, Heckel A, Rettig WJ (2008) BIBF 1120: triple angiokinase inhibitor with sustained receptor blockade and good antitumor efficacy. Cancer Res 68:4774–4782
7. Hostettler KE, Zhong J, Papakonstantinou E, Karakiulakis G, Tamm M, Seidel P, Sun Q, Mandal J, Lardinois D, Lambers C, Roth M (2014) Anti-fibrotic effects of nintedanib in lung fibroblasts derived from patients with idiopathic pulmonary fibrosis. Respir Res 15:157
8. Wollin L, Maillet I, Quesniaux V, Holweg A, Ryffel B (2014) Antifibrotic and anti-inflammatory activity of the tyrosine kinase inhibitor nintedanib in experimental models of lung fibrosis. J Pharmacol Exp Ther 349:209–220
9. Wollin L (2015) Mode of action of nintedanib in the treatment of idiopathic pulmonary fibrosis. Eur Respir J 45:1434–1445
10. Crino L, Metro G (2014) Therapeutic options targeting angiogenesis in nonsmall cell lung cancer. Eur Respir Rev 23:79–91
11. Renzoni EA (2004) Neovascularization in idiopathic pulmonary fibrosis: too much or too little? Am J Respir Crit Care Med 169:1179–1180
12. Ford NL, Martin EL, Lewis JF, Veldhuizen RA, Holdsworth DW, Drangova M (2009) Quantifying lung morphology with respiratory-gated micro-CT in a murine model of emphysema. Phys Med Biol 54:2121–2130
13. Artaechevarria X, Blanco D, Pérez-Martín D, de Biurrun G, Montuenga LM, de Torres JP, Zulueta JJ, Bastarrika G, Muñoz-Barrutia A, Ortiz-de-Solorzano C (2010) Longitudinal study of a mouse model of chronic pulmonary inflammation using breath hold gated micro-CT. Eur Radiol 20:2600–2608
14. Hübner RH, Gitter W, El Mokhtari NE, Mathiak M, Both M, Bolte H, Freitag-Wolf S, Bewig B (2008) Standardized quantification of pulmonary fibrosis in histological samples. Biotechniques 44:507–517
15. Richeldi L, du Bois RM, Raghu G, Azuma A, Brown KK, Costabel U, Cottin V, Flaherty KR, Hansell DM, Inoue Y, Kim DS, Kolb M, Nicholson AG, Noble PW, Selman M, Taniguchi H, Brun M, Le Maulf F, Girard M, Stowasser S, Schlenker-Herceg R, Disse B, Collard HR (2014) INPULSIS Trial Investigators: efficacy and safety of nintedanib in idiopathic pulmonary fibrosis. N Engl J Med 370:2071–2082
16. Richeldi L, Costabel U, Selman M, Kim DS, Hansell DM, Nicholson AG, Brown KK, Flaherty KR, Noble PW, Raghu G, Brun M, Gupta A, Juhel N, Klüglich M, du Bois RM (2011) Efficacy of a tyrosine kinase inhibitor in idiopathic pulmonary fibrosis. N Engl J Med 365:1079–1087
17. Moeller A, Ask K, Warburton D, Gauldie J, Kolb M (2008) The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis? Int J Biochem Cell Biol 40:362–382
18. Izbicki G, Segel MJ, Christensen TG, Conner MW, Breuer R (2002) Time course of bleomycin-induced lung fibrosis. Int J Exp Pathol 83:111–119
19. Wynn TA, Barron L (2010) Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 30:245–257
20. Pechkovsky DV, Prasse A, Kollert F, Engel KM, Dentler J, Luttmann W, Friedrich K, Müller-Quernheim J, Zissel G (2010) Alternatively activated alveolar macrophages in pulmonary fibrosis-mediator production and intracellular signal transduction. Clin Immunol 137:89–101
21. Schupp JC, Binder H, Jäger B, Cillis G, Zissel G, Müller-Quernheim J, Prasse A (2015) Macrophage activation in acute exacerbation of idiopathic pulmonary fibrosis. PLoS ONE 10:e0116775. doi:10.1371/journal.pone.0116775
22. Chamoto K, Gibney BC, Ackermann M, Lee GS, Konerding MA, Tsuda A, Mentzer SJ (2013) Alveolar epithelial dynamics in postpneumonectomy lung growth. Anat Rec (Hoboken) 296:495–503
23. Chamoto K, Gibney BC, Ackermann M, Lee GS, Lin M, Konerding MA, Tsuda A, Mentzer SJ (2012) Alveolar macrophage dynamics in murine lung regeneration. J Cell Physiol 227:3208–3215
24. Roth GJ, Binder R, Colbatzky F, Dallinger C, Schlenker-Herceg R, Hilberg F, Wollin SL, Kaiser R (2015) Nintedanib: from discovery to the clinic. J Med Chem 58:1053–1063
25. Hellberg C, Ostman A, Heldin CH (2010) PDGF and vessel maturation. Recent Results Cancer Res 180:103–114
26. Grimminger F, Günther A, Vancheri C (2015) The role of tyrosine kinases in the pathogenesis of idiopathic pulmonary fibrosis. Eur Respir J 45:1426–1433
27. Costabel U, Inoue Y, Richeldi L, Collard HR, Tschoepe I, Stowasser S, Azuma A (2016) Efficacy of nintedanib in idiopathic pulmonary fibrosis across prespecified subgroups in INPULSIS. Am J Respir Crit Care Med 193:178–185
28. Ueha S, Shand FH, Matsushima K (2012) Cellular and molecular mechanisms of chronic inflammation-associated organ fibrosis. Front Immunol 3:71
29. Strieter RM (2008) What differentiates normal lung repair and fibrosis? Inflammation, resolution of repair, and fibrosis. Proc Am Thorac Soc 5:305–310
30. Mentzer SJ, Konerding MA (2014) Intussusceptive angiogenesis: expansion and remodeling of microvascular networks. Angiogenesis 17:499–509
31. Ackermann M, Tsuda A, Secomb TW, Mentzer SJ, Konerding MA (2013) Intussusceptive remodeling of vascular branch angles in chemically-induced murine colitis. Microvasc Res 87:75–82
32. Ackermann M, Morse BA, Delventhal V, Carvajal IM, Konerding MA (2012) Anti-VEGFR2 and anti-IGF-1R-Adnectins inhibit Ewing’s sarcoma A673-xenograft growth and normalize tumor vascular architecture. Angiogenesis 15:685–695
33. Ackermann M, Houdek JP, Gibney BC, Ysasi A, Wagner W, Belle J, Schittny JC, Enzmann F, Tsuda A, Mentzer SJ, Konerding MA (2014) Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization. Angiogenesis 17:541–551
34. Smadja DM, Mauge L, Nunes H, d’Audigier C, Juvin K, Borie R, Carton Z, Bertil S, Blanchard A, Crestani B, Valeyre D, Gaussem P, Israel-Biet D (2013) Imbalance of circulating endothelial cells and progenitors in idiopathic pulmonary fibrosis. Angiogenesis 16:147–157
35. de García de Alba C, Buendia-Roldán I, Salgado A, Becerril C, Ramírez R, González Y, Checa M, Navarro C, Ruiz V, Pardo A, Selman M (2015) Fibrocytes contribute to inflammation and fibrosis in chronic hypersensitivity pneumonitis through paracrine effects. Am J Respir Crit Care Med 191:427–436
36. Schraufnagel DE, Mehta D, Harshbarger R, Treviranus K, Wang NS (1986) Capillary remodeling in bleomycin-induced pulmonary fibrosis. Am J Pathol 125:97–106
37. Hashimoto N, Phan SH, Imaizumi K, Matsuo M, Nakashima H, Kawabe T, Shimokata K, Hasegawa Y (2010) Endothelial-mesenchymal transition in bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 43:161–172