Emphysema and mechanical stress-induced lung remodeling

Physiology

Volumn 28, Issue 6, 2013, Pages 404-413

  Suki, Béla ^a   Sato, Susumu ^a   Parameswaran, Harikrishnan ^a   Szabari, Margit V ^a   Takahashi, Ayuko ^a   Bartolák Suki, Erzsébet ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AIRWAY REMODELING; ANIMAL; DISEASE COURSE; HUMAN; LUNG; LUNG EMPHYSEMA; MECHANICAL STRESS; MECHANOTRANSDUCTION; PATHOLOGY; PATHOPHYSIOLOGY; PRESSURE; PROGNOSIS; REVIEW;

AIRWAY REMODELING; ANIMALS; DISEASE PROGRESSION; HUMANS; LUNG; MECHANOTRANSDUCTION, CELLULAR; PRESSURE; PROGNOSIS; PULMONARY EMPHYSEMA; STRESS, MECHANICAL;

EID: 84887104993     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00041.2013     Document Type: Review

References (73)

1. Alencar AM, Arold SP, Buldyrev SV, Majumdar A, Stamenovic D, Stanley HE, Suki B. Physiology: dynamic instabilities in the inflating lung. Nature 417: 809-811, 2002.
2. Arold SP, Bartolak-Suki E, Suki B. Variable stretch pattern enhances surfactant secretion in alveolar type II cells in culture. Am J Physiol Lung Cell Mol Physiol 296: L574-L581, 2009.
3. Arold SP, Suki B, Alencar AM, Lutchen KR, Ingenito EP. Variable ventilation induces endogenous surfactant release in normal guinea pigs. Am J Physiol Lung Cell Mol Physiol 285: L370-L375, 2003.
4. Baglole CJ, Bushinsky SM, Garcia TM, Kode A, Rahman I, Sime PJ, Phipps RP. Differential induction of apoptosis by cigarette smoke extract in primary human lung fibroblast strains: implications for emphysema. Am J Physiol Lung Cell Mol Physiol 291: L19-L29, 2006.
5. Barnes PJ. Chronic obstructive pulmonary disease. N Engl J Med 343: 269-280, 2000.
6. Bartolák-Suki E, Suki B. Effects of glucose level and variability in stretch on fibroblast mitochondrial ATP-synthase from normal and emphysematous mouse lungs. Am J Respir Crit Care Med 187: A1887, 2013.
7. Boudreault F, Tschumperlin DJ. Stretch-induced mitogen-activated protein kinase activation in lung fibroblasts is independent of receptor tyrosine kinases. Am J Respir Cell Mol Biol 43: 64-73, 2010.
8. Breen EC. Mechanical strain increases type I collagen expression in pulmonary fibroblasts in vitro. J Appl Physiol 88: 203-209, 2000.
9. Brewer KK, Sakai H, Alencar AM, Majumdar A, Arold SP, Lutchen KR, Ingenito EP, Suki B. Lung and alveolar wall elastic and hysteretic behavior in rats: effects of in vivo elastase treatment. J Appl Physiol 95: 1926-1936, 2003.
10. Cardoso WV, Sekhon HS, Hyde DM, Thurlbeck WM. Collagen and elastin in human pulmonary emphysema. Am Rev Respir Dis 147: 975-981, 1993.
11. Cavalcante FS, Ito S, Brewer KK, Sakai H, Alencar AM, Almeida MP, Andrade JS Jr, Majumdar A, Ingenito EP, Suki B. Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. J Appl Physiol 98: 672-679, 2005.
12. Chiquet M, Gelman L, Lutz R, Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim Biophys Acta 1793: 911-920, 2009.
13. Churg A, Wang RD, Tai H, Wang X, Xie C, Dai J, Shapiro SD, Wright JL. Macrophage metalloelas-tase mediates acute cigarette smoke-induced inflammation via tumor necrosis factor-alpha release. Am J Respir Crit Care Med 167: 1083-1089, 2003.
14. Churg A, Wright JL. Proteases and emphysema. Curr Opin Pulm Med 11: 153-159, 2005.
15. Cosio MG, Majo J, Cosio MG. Inflammation of the airways and lung parenchyma in COPD: role of T cells. Chest 121: 160S-165S, 2002.
16. Demedts IK, Demoor T, Bracke KR, Joos GF, Brusselle GG. Role of apoptosis in the pathogen-esis of COPD and pulmonary emphysema. Respir Res 7: 53, 2006.
17. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689, 2006.
18. Foronjy RF, Okada Y, Cole R, D'Armiento J. Progressive adult-onset emphysema in transgenic mice expressing human MMP-1 in the lung. Am J Physiol Lung Cell Mol Physiol 284: L727-L737, 2003.
19. Gao F, Koenitzer JR, Tobolewski JM, Jiang D, Liang J, Noble PW, Oury TD. Extracellular super-oxide dismutase inhibits inflammation by preventing oxidative fragmentation of hyaluronan. J Biol Chem 283: 6058-6066, 2008.
20. Hakansson L, Venge P. The molecular basis of the hyaluronic acid-mediated stimulation of granulo-cyte function. J Immunol 138: 4347-4352, 1987.
21. Hantos Z, Adamicza A, Janosi TZ, Szabari MV, Tolnai J, Suki B. Lung volumes and respiratory mechanics in elastase-induced emphysema in mice. J Appl Physiol 105: 1864-1872, 2008.
22. Hawwa RL, Hokenson MA, Wang Y, Huang Z, Sharma S, Sanchez-Esteban J. Differential expression of MMP-2 and -9 and their inhibitors in fetal lung cells exposed to mechanical stretch: regulation by IL-10. Lung 189: 341-349, 2011.
23. Hayashi A, Ryu A, Suzuki T, Kawada A, Tajima S. In vitro degradation of tropoelastin by reactive oxygen species. Arch Dermatol Res 290: 497-500, 1998.
24. Hoffman AM, Shifren A, Mazan MR, Gruntman AM, Lascola KM, Nolen-Walston RD, Kim CF, Tsai L, Pierce RA, Mecham RP, Ingenito EP. Matrix modulation of compensatory lung regrowth and progenitor cell proliferation in mice. Am J Physiol Lung Cell Mol Physiol 298: L158-L168, 2010.
25. Houghton AM, Quintero PA, Perkins DL, Kobayashi DK, Kelley DG, Marconcini LA, Mecham RP, Senior RM, Shapiro SD. Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest 116: 753-759, 2006.
26. Hunninghake GW, Davidson JM, Rennard S, Szapiel S, Gadek JE, Crystal RG. Elastin fragments attract macrophage precursors to diseased sites in pulmonary emphysema. Science 212: 925-927, 1981.
27. Imai K, Dalal SS, Chen ES, Downey R, Schulman LL, Ginsburg M, D'Armiento J. Human collage-nase (matrix metalloproteinase-1) expression in the lungs of patients with emphysema. Am J Respir Crit Care Med 163: 786-791, 2001.
28. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J 20: 811-827, 2006.
29. Ito I, Nagai S, Handa T, Muro S, Hirai T, Tsukino M, Mishima M. Matrix metalloproteinase-9 promoter polymorphism associated with upper lung dominant emphysema. Am J Respir Crit Care Med 172: 1378-1382, 2005.
30. Ito S, Ingenito EP, Brewer KK, Black LD, Parameswaran H, Lutchen KR, Suki B. Mechanics, nonlinearity, and failure strength of lung tissue in a mouse model of emphysema: possible role of collagen remodeling. J Appl Physiol 98: 503-511, 2005.
31. Janmey PA, Winer JP, Murray ME, Wen Q. The hard life of soft cells. Cell Motil Cytoskeleton 66: 597-605, 2009.
32. Jesudason R, Sato S, Parameswaran H, Araujo AD, Majumdar A, Allen PG, Bartolak-Suki E, Suki B. Mechanical forces regulate elastase activity and binding site availability in lung elastin. Bio-phys J 99: 3076-3083, 2010.
33. Kliment CR, Tobolewski JM, Manni ML, Tan RJ, Enghild J, Oury TD. Extracellular superoxide dis-mutase protects against matrix degradation of heparan sulfate in the lung. Antioxidants Redox Signal 10: 261-268, 2008.
34. Kononov S, Brewer K, Sakai H, Cavalcante FS, Sabayanagam CR, Ingenito EP, Suki B. Roles of mechanical forces and collagen failure in the development of elastase-induced emphysema. Am J Respir Crit Care Med 164: 1920-1926, 2001.
35. Kuratomi Y, Okazaki N, Ishihara T, Arai T, Kira S. Variability of breath-by-breath tidal volume and its characteristics in normal and diseased subjects. Ventilatory monitoring with electrical impedance pneumography. Japan J Med 24: 141-149, 1985.
36. Laurent GJ, Chambers RC, Hill MR, McAnulty RJ. Regulation of matrix turnover: fibroblasts, forces, factors and fibrosis. Biochem Soc Trans 35: 647-651, 2007.
37. Lavietes MH, Smeltzer SC, Cook SD, Modak RM, Smaldone GC. Airway dynamics, oesophageal pressure and cough. Eur Respir J 11: 156-161, 1998.
38. Lee JH, Hanaoka M, Kitaguchi Y, Kraskauskas D, Shapiro L, Voelkel NF, Taraseviciene-Stewart L. Imbalance of apoptosis and cell proliferation contributes to the development and persistence of emphysema. Lung 190: 69-82, 2012.
39. Liu F, Mih JD, Shea BS, Kho AT, Sharif AS, Tager AM, Tschumperlin DJ. Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 190: 693-706, 2010.
40. McDonough JE, Yuan R, Suzuki M, Seyednejad N, Elliott WM, Sanchez PG, Wright AC, Gefter WB, Litzky L, Coxson HO, Pare PD, Sin DD, Pierce RA, Woods JC, McWilliams AM, Mayo JR, Lam SC, Cooper JD, Hogg JC. Small-airway obstruction and emphysema in chronic obstructive pulmonary disease. N Engl J Med 365: 1567-1575, 2011.
41. Merrilees MJ, Ching PS, Beaumont B, Hinek A, Wight TN, Black PN. Changes in elastin, elastin binding protein and versican in alveoli in chronic obstructive pulmonary disease. Respir Res 9: 41, 2008.
42. Mohamed Hoesein FA, Zanen P, de Jong PA, van Ginneken B, Boezen HM, Groen HJ, Oudkerk M, de Koning HJ, Postma DS, Lammers JW. Rate of progression of CT-quantified emphysema in male current and ex-smokers: a follow-up study. Re-spir Res 14: 55, 2013.
43. Mouded M, Egea EE, Brown MJ, Hanlon SM, Houghton AM, Tsai LW, Ingenito EP, Shapiro SD. Epithelial cell apoptosis causes acute lung injury masquerading as emphysema. Am J Respir Cell Mol Biol 41: 407-414, 2009.
44. Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT. Matrix metalloproteinase-medi-ated extracellular matrix protein degradation in human pulmonary emphysema. Lab Invest 78: 1077-1087, 1998.
45. Osman M, Keller S, Hosannah Y, Cantor JO, Turino GM, Mandl I. Impairment of elastin resyn-thesis in the lungs of hamsters with experimental emphysema induced by sequential administration of elastase and trypsin. J Lab Clin Med 105: 254-258, 1985.
46. Overbeek SA, Braber S, Koelink PJ, Henricks PA, Mortaz E, LoTam Loi AT, Jackson PL, Garssen J, Wagenaar GT, Timens W, Koenderman L, Blalock JE, Kraneveld AD, Folkerts G. Cigarette smoke-induced collagen destruction; key to chronic neu-trophilic airway inflammation? PLos One 8: e55612, 2013.
47. Parameswaran H, Majumdar A, Suki B. Linking microscopic spatial patterns of tissue destruction in emphysema to macroscopic decline in stiffness using a 3D computational model. PLos Comput Biol 7: e1001125, 2011.
48. Retamales I, Elliott WM, Meshi B, Coxson HO, Pare PD, Sciurba FC, Rogers RM, Hayashi S, Hogg JC. Amplification of inflammation in emphysema and its association with latent adenovi-ral infection. Am J Respir Crit Care Med 164: 469-473, 2001.
49. Sakai H, Ingenito EP, Mora R, Abbay S, Caval-cante FS, Lutchen KR, Suki B. Hysteresivity of the lung and tissue strip in the normal rat: effects of heterogeneities. J Appl Physiol 91: 737-747, 2001.
50. Seemungal TA, Harper-Owen R, Bhowmik A, Jeffries DJ, Wedzicha JA. Detection of rhinovirus in induced sputum at exacerbation of chronic obstructive pulmonary disease. Eur Respir J 16: 677-683, 2000.
51. Shapiro SD. Elastolytic metalloproteinases produced by human mononuclear phagocytes. Potential roles in destructive lung disease. Am J Respir Crit Care Med 150: S160-S164, 1994.
52. Shapiro SD, Senior Matrix metalloproteinases RM. Matrix degradation and more. Am J Respir Cell Mol Biol 20: 1100-1102, 1999.
53. Shyy JY, Chien S. Role of integrins in endothelial mechanosensing of shear stress. Circ Res 91: 769-775, 2002.
54. Smith JC, Butler JP, Hoppin FG Jr. Contribution of tree structures in the lung to lung elastic recoil. J Appl Physiol 57: 1422-1429, 1984.
55. Song J, Hu B, Qu H, Bi C, Huang X, Zhang M. Mechanical stretch modulates microRNA 21 expression, participating in proliferation and apop-tosis in cultured human aortic smooth muscle cells. PLos One 7: e47657, 2012.
56. Stockley RA, O'Brien C, Pye A, Hill SL. Relationship of sputum color to nature and outpatient management of acute exacerbations of COPD. Chest 117: 1638-1645, 2000.
57. Suki B, Barabasi AL, Hantos Z, Petak F, Stanley HE. Avalanches and power-law behaviour in lung inflation. Nature 368: 615-618, 1994.
58. Suki B, Ito S, Stamenovic D, Lutchen KR, Ingenito EP. Biomechanics of the lung parenchyma: critical roles of collagen and mechanical forces. J Appl Physiol 98: 1892-1899, 2005.
59. Suki B, Lutchen KR, Ingenito EP. On the progressive nature of emphysema: roles of proteases, inflammation, and mechanical forces. Am J Re-spir Crit Care Med 168: 516-521, 2003.
60. Suki B, Stamenovic D, Hubmayr RD. Lung parenchy-mal mechanics. In: Comprehensive Physiology, The Respiratory System, Respiration Mechanics: Organ, Cell, Molecule, Edited by Fredberg JJ, Sieck GC, Gerthoffer WT. Hoboken, NJ: Wiley-Blackwell, 2011, p. 1317-1351.
61. Szabari MV, Parameswaran H, Sato S, Hantos Z, Bartolak-Suki E, Suki B. Acute mechanical forces cause deterioration in lung structure and function in elastase-induced emphysema. Am J Physiol Lung Cell Mol Physiol 303: L567-L574, 2012.
62. Tanabe N, Muro S, Hirai T, Oguma T, Terada K, Marumo S, Kinose D, Ogawa E, Hoshino Y, Mishima M. Impact of exacerbations on emphysema progression in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 183: 1653-1659, 2011.
63. Taraseviciene-Stewart L, Voelkel NF. Molecular pathogenesis of emphysema. J Clin Invest 118: 394-402, 2008.
64. Togo S, Holz O, Liu X, Sugiura H, Kamio K, Wang X, Kawasaki S, Ahn Y, Fredriksson K, Skold CM, Mueller KC, Branscheid D, Welker L, Watz H, Magnussen H, Rennard SI. Lung fibroblast repair functions in patients with chronic obstructive pulmonary disease are altered by multiple mechanisms. Am J Respir Crit Care Med 178: 248-260, 2008.
65. Tolnai J, Szabari MV, Albu G, Maar BA, Parameswaran H, Bartolak-Suki E, Suki B, Hantos Z. Functional and morphological assessment of early impairment of airway function in a rat model of emphysema. J Appl Physiol 112: 1932-1939, 2012.
66. Tschumperlin DJ, Margulies SS. Alveolar epithelial surface area-volume relationship in isolated rat lungs. J Appl Physiol 86: 2026-2033, 1999.
67. van Straaten JF, Coers W, Noordhoek JA, Hu-itema S, Flipsen JT, Kauffman HF, Timens W, Postma DS. Proteoglycan changes in the extracellular matrix of lung tissue from patients with pulmonary emphysema. Mod Pathol 12: 697-705, 1999.
68. West JB. Distribution of mechanical stress in the lung, a possible factor in localisation of pulmonary disease. Lancet 1: 839-841, 1971.
69. West JB, Mathieu-Costello O. Strength of the pulmonary blood-gas barrier. Respir Physiol 88: 141-148, 1992.
70. Winkler T, Suki B. Emergent structure-function relations in emphysema and asthma. Crit Rev Biomed Eng 39: 263-280, 2011.
71. Wirtz HR, Dobbs LG. Calcium mobilization and exocytosis after one mechanical stretch of lung epithelial cells. Science 250: 1266-1269, 1990.
72. Wright JL. Airway inflammatory cells in upper and lower lobes in lungs of patients with and without emphysema. Pathol Res Practice 183: 297-300, 1988.
73. Yao H, Arunachalam G, Hwang JW, Chung S, Sundar IK, Kinnula VL, Crapo JD, Rahman I. Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc Natl Acad Sci USA 107: 15571-15576, 2010.