Linking progression of fibrotic lung remodeling and ultrastructural alterations of alveolar epithelial type II cells in the amiodarone mouse model

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 1, 2015, Pages L63-L75

  Birkelbach, Bastian ^a,b,d   Lutz, Dennis ^a,b,d   Ruppert, Clemens ^c,d   Henneke, Ingrid ^c,d   Lopez Rodriguez, Elena ^a,b,d   Günther, Andreas ^c,d,e,f,g   Ochs, Matthias ^a,b,d,h   Mahavadi, Poornima ^c,d   Knudsen, Lars ^a,b,d  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Biomedical Research in Endstage and Obstructive Lung Disease (BREATH)   (Germany)

^c JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^d German Center for Lung Research (DZL)   (Germany)

^e European IPF Network   (Germany)

^f Department of Cardiac Pathobiology   (Germany)

^g Agaplesion Lung Clinic Waldhof Elgershausen   (Germany)

^h Excellence Cluster REBIRTH   (Germany)

Author keywords

Alveolar epithelial type II cells; Collapse induration; Pulmonary fibrosis; Stereology; Surfactant

Indexed keywords

AMIODARONE; COLLAGEN; LUNG SURFACTANT; VASODILATOR AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATELECTASIS; CELL STRESS; CELL ULTRASTRUCTURE; CELL VOLUME; COLLAGEN FIBRIL; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; FIBROGENESIS; FIBROSING ALVEOLITIS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LAMELLAR BODY; LUNG ALVEOLUS EPITHELIUM CELL; LUNG PARENCHYMA; MACROAUTOPHAGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; QUALITATIVE ANALYSIS; STEREOLOGY; AIRWAY REMODELING; ANIMAL; C57BL MOUSE; CELL SIZE; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; EPITHELIUM CELL; LUNG ALVEOLUS; MALE; METABOLISM; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA;

AIRWAY REMODELING; AMIODARONE; ANIMALS; APOPTOSIS; CELL SIZE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; MALE; MICE; MICE, INBRED C57BL; ORGAN CULTURE TECHNIQUES; PULMONARY ALVEOLI; PULMONARY SURFACTANTS; RESPIRATORY MUCOSA; VASODILATOR AGENTS;

EID: 84936141052     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00279.2014     Document Type: Article

References (64)

1. Araya J, Kojima J, Takasaka N, Ito S, Fujii S, Hara H, Yanagisawa H, Kobayashi K, Tsurushige C, Kawaishi M, Kamiya N, Hirano J, Odaka M, Morikawa T, Nishimura SL, Kawabata Y, Hano H, Na-kayama K, Kuwano K. Insufficient autophagy in idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 304: L56–L69, 2013.
2. Atochina-Vasserman EN, Bates SR, Zhang P, Abramova H, Zhang Z, Gonzales L, Tao JQ, Gochuico BR, Gahl W, Guo CJ, Gow AJ, Beers MF, Guttentag S. Early alveolar epithelial dysfunction promotes lung inflammation in a mouse model of Hermansky-Pudlak syndrome. Am J Respir Crit Care Med 184: 449–458, 2011.
3. Bachofen H, Schürch S. Alveolar surface forces and lung architecture. Comp Biochem Physiol A Mol Integr Physiol 129: 183–193, 2001.
4. Bargout R, Jankov A, Dincer E, Wang R, Komodromos T, Ibarra-Sunga O, Filippatos G, Uhal BD. Amiodarone induces apoptosis of human and rat alveolar epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 278: L1039–L1044, 2000.
5. Beers MF, Hawkins A, Maguire JA, Kotorashvili A, Zhao M, Newitt JL, Ding W, Russo S, Guttentag S, Gonzales L, Mulugeta S. A nonaggregating surfactant protein C mutant is misdirected to early endo-somes and disrupts phospholipid recycling. Traffic 12: 1196–1210, 2011.
6. Carloni A, Poletti V, Fermo L, Bellomo N, Chilosi M. Heterogeneous distribution of mechanical stress in human lung: a mathematical approach to evaluate abnormal remodeling in IPF. J Theor Biol 332: 136–140, 2013.
7. Charles PE, Doise JM, Quenot JP, Muller G, Aube H, Baudouin N, Piard F, Besancenot JF, Blettery B. Amiodarone-related acute respiratory distress syndrome following sudden withdrawal of steroids. Respiration 73: 248–249, 2006.
8. Chilosi M, Carloni A, Rossi A, Poletti V. Premature lung aging and cellular senescence in the pathogenesis of idiopathic pulmonary fibrosis and COPD/emphysema. Transl Res 162: 156–173, 2013.
9. Coxson HO, Hogg JC, Mayo JR, Behzad H, Whittall KP, Schwartz DA, Hartley PG, Galvin JR, Wilson JS, Hunninghake GW. Quantification of idiopathic pulmonary fibrosis using computed tomography and histology. Am J Respir Crit Care Med 155: 1649–1656, 1997.
10. Fehrenbach H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2: 33–46, 2001.
11. Furuyama A, Kimata K, Mochitate K. Assembly of basement membrane in vitro by cooperation between alveolar epithelial cells and pulmonary fibroblasts. Cell Struct Funct 22: 603–614, 1997.
12. Gazdhar A, Temuri A, Knudsen L, Gugger M, Schmid RA, Ochs M, Geiser T. Targeted gene transfer of hepatocyte growth factor to alveolar type II epithelial cells reduces lung fibrosis in rats. Hum Gene Ther 24: 105–116, 2013.
13. Geiser T. Idiopathic pulmonary fibrosis–a disorder of alveolar wound repair? Swiss Med Wkly 133: 405–411, 2003.
14. Gundersen H, Jensen E. Stereological estimation of the volume-weighted mean volume of arbitrary particles observed on random sections. J Microsc 138: 127–142, 1985.
15. Günther A, Korfei M, Mahavadi P, von der Beck D, Ruppert C, Markart P. Unravelling the progressive pathophysiology of idiopathic pulmonary fibrosis. Eur Respir Rev 21: 152–160, 2012.
16. Günther A, Schmidt R, Nix F, Yabut-Perez M, Guth C, Rosseau S, Siebert C, Grimminger F, Morr H, Velcovsky H, Seeger W. Surfactant abnormalities in idiopathic pulmonary fibrosis, hypersensitivity pneumo-nitis and sarcoidosis. Eur Respir J 14: 565–573, 1999.
17. Guttentag SH, Akhtar A, Tao JQ, Atochina E, Rusiniak ME, Swank RT, Bates SR. Defective surfactant secretion in a mouse model of Hermansky-Pudlak syndrome. Am J Respir Cell Mol Biol 33: 14–21, 2005.
18. Hamvas A, Nogee LM, White FV, Schuler P, Hackett BP, Huddleston CB, Mendeloff EN, Hsu FF, Wert SE, Gonzales LW, Beers MF, Ballard PL. Progressive lung disease and surfactant dysfunction with a deletion in surfactant protein C gene. Am J Respir Cell Mol Biol 30: 771–776, 2004.
19. Horiuchi T, Ikegami M, Cherniack RM, Mason RJ. Increased surface tension of the lung and surfactant in bleomycin-induced pulmonary fibro-sis in rats. Am J Respir Crit Care Med 154: 1002–1005, 1996.
20. Horowitz JC, Thannickal VJ. Epithelial-mesenchymal interactions in pulmonary fibrosis. Semin Respir Crit Care Med 27: 600–612, 2006.
21. Hsia C, Hyde D, Ochs M, Weibel E. An official research policy statement of the American Thoracic Society/European Respiratory Society: standards for quantitative assessment of lung structure. Am J Respir Crit Care Med 181: 394–418, 2010.
22. Hyde DM, Tyler NK, Putney LF, Singh P, Gundersen HJ. Total number and mean size of alveoli in mammalian lung estimated using fractionator sampling and unbiased estimates of the Euler characteristic of alveolar openings. Anat Rec A Discov Mol Cell Evol Biol 277: 216–226, 2004.
23. Kawanami O, Ferrans VJ, Crystal RG. Structure of alveolar epithelial cells in patients with fibrotic lung disorders. Lab Invest 46: 39–53, 1982.
24. Knudsen L, Waizy H, Fehrenbach H, Richter J, Wahlers T, Wittwer T, Ochs M. Ultrastructural changes of the intracellular surfactant pool in a rat model of lung transplantation-related events. Respir Res 12: 79, 2011.
25. Königshoff M, Kramer M, Balsara N, Wilhelm J, Amarie O, Jahn A, Rose F, Fink L, Seeger W, Schaefer L, Günther A, Eickelberg O. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest 119: 772–787, 2009.
26. Korfei M, Ruppert C, Mahavadi P, Henneke I, Markart P, Koch M, Lang G, Fink L, Bohle R, Seeger W, Weaver T, Guenther A. Epithelial endoplasmic reticulum stress and apoptosis in sporadic idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 178: 838–846, 2008.
27. Korfei M, von der Beck D, Henneke I, Markart P, Ruppert C, Mahavadi P, Ghanim B, Klepetko W, Fink L, Meiners S, Krämer OH, Seeger W, Vancheri C, Guenther A. Comparative proteome analysis of lung tissue from patients with idiopathic pulmonary fibrosis (IPF), nonspecific interstitial pneumonia (NSIP) and organ donors. J Proteomics 85: 109–128, 2013.
28. Kuhn C, Boldt J, King TE, Crouch E, Vartio T, McDonald JA. An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis. Am Rev Respir Dis 140: 1693–1703, 1989.
29. Lazenby A, Crouch E, McDonald J, Kuhn C 3rd. Remodeling of the lung in bleomycin-induced pulmonary fibrosis in the rat. An immunohis-tochemical study of laminin, type IV collagen, and fibronectin. Am Rev Respir Dis 142: 206–214, 1990.
30. Leuenberger A, Gazdhar A, Herrmann G, Ochs M, Geiser T, Knud-sen L. Cell-specific expression of human HGF by alveolar type II cells induces remodeling of septal wall tissue in the lung: a morphometric study. J Appl Physiol 113: 799–807, 2012.
31. Lutz D, Gazdhar A, Lopez-Rodriguez E, Ruppert C, Mahavadi P, Günther A, Klepetko W, Bates JH, Smith B, Geiser T, Ochs M, Knudsen L. Alveolar derecruitment and collapse induration as crucial mechanisms in lung injury and fibrosis. Am J Respir Cell Mol Biol 52: 232–243, 2015.
32. Mahavadi P, Knudsen L, Venkatesan S, Henneke I, Hegermann J, Wrede C, Ochs M, Ahuja A, Chillappagari S, Ruppert C, Seeger W, Korfei M, Guenther A. Regulation of macroautophagy in amiodarone induced pulmonary fibrosis. J Pathol. In press.
33. Mahavadi P, Henneke I, Ruppert C, Knudsen L, Venkatesan S, Liebisch G, Chambers RC, Ochs M, Schmitz G, Vancheri C, Seeger W, Korfei M, Guenther A. Altered surfactant homeostasis and alveolar epithelial cell stress in amiodarone-induced lung fibrosis. Toxicol Sci 142: 285–297, 2014.
34. Mahavadi P, Korfei M, Henneke I, Liebisch G, Schmitz G, Gochuico BR, Markart P, Bellusci S, Seeger W, Ruppert C, Guenther A. Epithelial stress and apoptosis underlie Hermansky-Pudlak syndrome-associated interstitial pneumonia. Am J Respir Crit Care Med 182: 207–219, 2010.
35. Majno G, Joris I. Apoptosis, oncosis, necrosis. An overview of cell death. Am J Pathol 146: 3–15, 1995.
36. Mühlfeld C, Ochs M. Quantitative microscopy of the lung: a problem-based approach. Part 2: stereological parameters and study designs in various diseases of the respiratory tract. Am J Physiol Lung Cell Mol Physiol 305: L205–L221, 2013.
37. Mulugeta S, Nguyen V, Russo S, Muniswamy M, Beers M. A surfactant protein C precursor protein BRICHOS domain mutation causes endoplas-mic reticulum stress, proteasome dysfunction, and caspase 3 activation. Am J Respir Cell Mol Biol 32: 521–530, 2005.
38. Myers J, Katzenstein A. Epithelial necrosis and alveolar collapse in the pathogenesis of usual interstitial pneumonia. Chest 94: 1309–1311, 1988.
39. Nogee L, Dunbar Ar Wert S, Askin F, Hamvas A, Whitsett J. A mutation in the surfactant protein C gene associated with familial interstitial lung disease. N Engl J Med 344: 573–579, 2001.
40. Ochs M, Mühlfeld C. Quantitative microscopy of the lung: a problem-based approach. Part 1: basic principles of lung stereology. Am J Physiol Lung Cell Mol Physiol 305: L15–L22, 2013.
41. Ochs M, Nyengaard JR, Jung A, Knudsen L, Voigt M, Wahlers T, Richter J, Gundersen HJ. The number of alveoli in the human lung. Am J Respir Crit Care Med 169: 120–124, 2004.
42. Perez-Gil J, Weaver TE. Pulmonary surfactant pathophysiology: current models and open questions. Physiology (Bethesda) 25: 132–141, 2010.
43. 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, Müller NL, Nicholson AG, Richeldi L, Selman M, Dudden RF, Griss BS, Protzko SL, Schünemann HJ; ATS/ERS/JRS/ALAT Committee on Idiopathic Pulmonary Fibrosis. 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, 2011.
44. Ruppert C, Kuchenbuch T, Boensch M, Schmidt S, Mathes U, Hill-ebrand V, Henneke I, Markart P, Reiss I, Schermuly RT, Seeger W, Günther A. Dry powder aerosolization of a recombinant surfactant protein-C-based surfactant for inhalative treatment of the acutely inflamed lung. Crit Care Med 38: 1584–1591, 2010.
45. Scherle W. A simple method for volumetry of organs in quantitative stereology. Mikroskopie 26: 57–60, 1970.
46. Schmidt R, Meier U, Markart P, Grimminger F, Velcovsky H, Morr H, Seeger W, Günther A. Altered fatty acid composition of lung surfactant phospholipids in interstitial lung disease. Am J Physiol Lung Cell Mol Physiol 283: L1079–L1085, 2002.
47. Schneider JP, Ochs M. Alterations of mouse lung tissue dimensions during processing for morphometry: a comparison of methods. Am J Physiol Lung Cell Mol Physiol 306: L341–L350, 2014.
48. Selman M, Pardo A. Role of epithelial cells in idiopathic pulmonary fibrosis: from innocent targets to serial killers. Proc Am Thorac Soc 3: 364–372, 2006.
49. Selman M, Pardo A, Richeldi L, Cerri S. Emerging drugs for idiopathic pulmonary fibrosis. Expert Opin Emerg Drugs 16: 341–362, 2011.
50. Sirianni FE, Chu FS, Walker DC. Human alveolar wall fibroblasts directly link epithelial type 2 cells to capillary endothelium. Am J Respir Crit Care Med 168: 1532–1537, 2003.
51. Sisson T, Mendez M, Choi K, Subbotina N, Courey A, Cunningham A, Dave A, Engelhardt J, Liu X, White E, Thannickal V, Moore B, Christensen P, Simon R. Targeted injury of type II alveolar epithelial cells induces pulmonary fibrosis. Am J Respir Crit Care Med 181: 254–263, 2010.
52. Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134: 127–136, 1984.
53. Tandrup T, Gundersen HJ, Jensen EB. The optical rotator. J Microsc 186: 108–120, 1997.
54. Tschanz S, Schneider JP, Knudsen L. Design-based stereology: planning, volumetry and sampling are crucial steps for a successful study. Ann Anat 196: 3–11, 2014.
55. Tschanz SA, Burri PH, Weibel ER. A simple tool for stereological assessment of digital images: the STEPanizer. J Microsc 243: 47–59, 2011.
56. Vasilescu DM, Knudsen L, Ochs M, Weibel ER, Hoffman EA. Optimized murine lung preparation for detailed structural evaluation via micro computed tomography. J Appl Physiol 112: 159–166, 2012.
57. Volckaert T, De Langhe S. Lung epithelial stem cells and their niches: Fgf10 takes center stage. Fibrogenesis Tissue Repair 7: 8, 2014.
58. Waisberg D, Barbas-Filho J, Parra E, Fernezlian S, Ribeiro de Carvalho C, Kairalla R, Capelozzi V. Abnormal expression of telom-erase/apoptosis limits type II alveolar epithelial cell replication in the early remodeling of usual interstitial pneumonia/idiopathic pulmonary fibrosis. Hum Pathol 41: 385–391, 2010.
59. Weaver TE, Na CL, Stahlman M. Biogenesis of lamellar bodies, lysosome-related organelles involved in storage and secretion of pulmonary surfactant. Semin Cell Dev Biol 13: 263–270, 2002.
60. Weibel E, Knight B. A morphometric study on the thickness of the pulmonary air-blood barrier. J Cell Biol 21: 367–396, 1964.
61. Weibel ER. It takes more than cells to make a good lung. Am J Respir Crit Care Med 187: 342–346, 2013.
62. Williams K, Malarkey D, Cohn L, Patrick D, Dye J, Toews G. Identification of spontaneous feline idiopathic pulmonary fibrosis: morphology and ultrastructural evidence for a type II pneumocyte defect. Chest 125: 2278–2288, 2004.
63. Wilson TA, Bachofen H. A model for mechanical structure of the alveolar duct. J Appl Physiol 52: 1064–1070, 1982.
64. Young LR, Gulleman PM, Bridges JP, Weaver TE, Deutsch GH, Blackwell TS, McCormack FX. The alveolar epithelium determines susceptibility to lung fibrosis in Hermansky-Pudlak syndrome. Am J Respir Crit Care Med 186: 1014–1024, 2012.