A role for matrix metalloproteinase 9 in IFNγ-mediated injury in developing lungs: Relevance to bronchopulmonary dysplasia

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 5, 2011, Pages 621-630

  Harijith, Anantha ^a,b   Choo Wing, Rayman ^a   Cataltepe, Sule ^c   Yasumatsu, Ryuji ^c,f   Aghai, Zubair H ^d   Janèr, Joakim ^e   Andersson, Sture ^e   Homer, Robert J ^a   Bhandari, Vineet ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Columbia University ^*  (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d Division of Female Pelvic Medicine and Reconstructive Surgery   (United States)

^e UNIVERSITY OF HELSINKI   (Finland)

^f KYUSHU UNIVERSITY   (Japan)

Author keywords

BPD; Hyperoxia; IFN ; MMP9; Newborn

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; CASPASE 3; CASPASE 6; CASPASE 8; CASPASE 9; CATHEPSIN B; CATHEPSIN H; CATHEPSIN K; CATHEPSIN L; CATHEPSIN S; CXCL11 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GELATINASE A; GELATINASE B; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE 14; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; CELL DEATH; CONTROLLED STUDY; HYPEROXIA; LUNG ALVEOLUS CELL; LUNG DYSPLASIA; LUNG INJURY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN TARGETING; SURVIVAL RATE; UPREGULATION;

ANGIOPOIETINS; ANIMALS; BRONCHOPULMONARY DYSPLASIA; CASPASES; CATHEPSINS; CHEMOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYPEROXIA; INFANT, NEWBORN; INTERFERON-GAMMA; LUNG INJURY; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; PAPIO; PHENOTYPE;

MURINAE; MUS; PAPIO;

EID: 79955491537     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0058OC     Document Type: Article

References (55)

1. Bhandari A, Bhandari V. Pitfalls, problems, and progress in bronchopulmonary dysplasia. Pediatrics 2009;123:1562-1573.
2. Bhandari A, Bhandari V. Pathogenesis, pathology and pathophysiology of pulmonary sequelae of bronchopulmonary dysplasia in premature infants. Front Biosci 2003;8:e370-e380.
3. Dickie R, Wang YT, Butler JP, Schulz H, Tsuda A. Distribution and quantity of contractile tissue in postnatal development of rat alveolar interstitium. Anat Rec (Hoboken) 2008;291:83-93.
4. Mokres LM, Parai K, Hilgendorff A, Ertsey R, Alvira CM, Rabinovitch M, Bland RD. Prolonged mechanical ventilation with air induces apoptosis and causes failure of alveolar septation and angiogenesis in lungs of newborn mice. Am J Physiol Lung Cell Mol Physiol 2010;298: L23-L35.
5. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004; 75:163-189. (Pubitemid 38174573)
6. Tellides G, Tereb DA, Kirkiles-Smith NC, Kim RW, Wilson JH, Schechner JS, Lorber MI, Pober JS. Interferon-gamma elicits arteriosclerosis in the absence of leukocytes. Nature 2000;403:207-211. (Pubitemid 30050965)
7. Bouma G, Strober W. The immunological and genetic basis of in- flammatory bowel disease. Nat Rev Immunol 2003;3:521-533. (Pubitemid 37328672)
8. Lundin KE, Nilsen EM, Scott HG, Loberg EM, Gjoen A, Bratlie J, Skar V, Mendez E, Lovik A, Kett K. Oats induced villous atrophy in coeliac disease. Gut 2003;52:1649-1652. (Pubitemid 37363452)
9. Vervoordeldonk MJ, Tak PP. Cytokines in rheumatoid arthritis. Curr Rheumatol Rep 2002;4:208-217.
10. Jensen JC, Pogrebniak HW, Pass HI, Buresh C, Merino MJ, Kauffman D, Venzon D, Langstein HN, Norton JA. Role of tumor necrosis factor in oxygen toxicity. J Appl Physiol 1992;72:1902-1907.
11. Shea LM, Beehler C, Schwartz M, Shenkar R, Tuder R, Abraham E. Hyperoxia activates NF-kappaB and increases TNF-alpha and IFNgamma gene expression in mouse pulmonary lymphocytes. J Immunol 1996;157:3902-3908. (Pubitemid 126449298)
12. Kim KB, Choi YH, Kim IK, Chung CW, Kim BJ, Park YM, Jung YK. Potentiation of Fas- and TRAIL-mediated apoptosis by IFN-gamma in A549 lung epithelial cells: enhancement of caspase-8 expression through IFN-response element. Cytokine 2002;20:283-288. (Pubitemid 36299048)
13. Vartanian T, Li Y, Zhao M, Stefansson K. Interferon-gamma-induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Mol Med 1995;1:732-743. (Pubitemid 3013083)
14. Wen LP, Madani K, Fahrni JA, Duncan SR, Rosen GD. Dexamethasone inhibits lung epithelial cell apoptosis induced by IFN-gamma and Fas. Am J Physiol 1997;273:L921-L929.
15. Wu AJ, Chen ZJ, Tsokos M, O'Connell BC, Ambudkar IS, Baum BJ. Interferon-gamma induced cell death in a cultured human salivary gland cell line. J Cell Physiol 1996;167:297-304. (Pubitemid 26145863)
16. Chen ES, Greenlee BM, Wills-Karp M, Moller DR. Attenuation of lung inflammation and fibrosis in interferon-gamma-deficient mice after intratracheal bleomycin. Am J Respir Cell Mol Biol 2001;24:545-555. (Pubitemid 32442761)
17. Segel MJ, Izbicki G, Cohen PY, Or R, Christensen TG, Wallach-Dayan SB, Breuer R. Role of interferon-gamma in the evolution of murine bleomycin lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2003; 285:L1255-L1262. (Pubitemid 37448796)
18. Saetta M, Mariani M, Panina-Bordignon P, Turato G, Buonsanti C, Baraldo S, Bellettato CM, Papi A, Corbetta L, Zuin R, et al. Increased expression of the chemokine receptor CXCR3 and its ligand CXCL10 in peripheral airways of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002;165:1404-1409. (Pubitemid 34522945)
19. +ve cells in the lungs of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999;160:711-717.
20. O'Shaughnessy TC, Ansari TW, Barnes NC, Jeffery PK. Inflammation in bronchial biopsies of subjects with chronic bronchitis: inverse relationship of CD8+ T lymphocytes with FEV1. Am J Respir Crit Care Med 1997;155:852-857. (Pubitemid 27133393)
21. Cosio MG, Guerassimov A. Chronic obstructive pulmonary disease: inflammation of small airways and lung parenchyma. Am J Respir Crit Care Med 1999;160:S21-S25.
22. Grumelli S, Corry DB, Song LZ, Song L, Green L, Huh J, Hacken J, Espada R, Bag R, Lewis DE, et al. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med 2004;1:e8.
23. Wang Z, Zheng T, Zhu Z, Homer RJ, Riese RJ, Chapman HA Jr, Shapiro SD, Elias JA. Interferon gamma induction of pulmonary emphysema in the adult murine lung. J Exp Med 2000;192:1587-1600.
24. Yamada M, Kubo H, Kobayashi S, Ishizawa K, Sasaki H. Interferongamma: a key contributor to hyperoxia-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2004;287:L1042-L1047. (Pubitemid 39391035)
25. Albertine KH, Jones GP, Starcher BC, Bohnsack JF, Davis PL, Cho SC, Carlton DP, Bland RD. Chronic lung injury in preterm lambs: disordered respiratory tract development. Am J Respir Crit Care Med 1999;159:945-958. (Pubitemid 29137801)
26. Buckley S, Warburton D. Dynamics of metalloproteinase-2 and -9, TGFbeta, and uPA activities during normoxic vs. hyperoxic alveolarization. Am J Physiol Lung Cell Mol Physiol 2002;283:L747-L754.
27. Chetty A, Cao GJ, Severgnini M, Simon A, Warburton R, Nielsen HC. Role of matrix metalloprotease-9 in hyperoxic injury in developing lung. Am J Physiol Lung Cell Mol Physiol 2008;295:L584-L592.
28. Ekekezie II, Thibeault DW, Simon SD, Norberg M, Merrill JD, Ballard RA, Ballard PL, Truog WE. Low levels of tissue inhibitors of metalloproteinases with a high matrix metalloproteinase-9/tissue inhibitor of metalloproteinase-1 ratio are present in tracheal aspirate fluids of infants who develop chronic lung disease. Pediatrics 2004;113: 1709-1714. (Pubitemid 38697980)
29. Cederqvist K, Sorsa T, Tervahartiala T, Maisi P, Reunanen K, Lassus P, Andersson S. Matrix metalloproteinases-2, -8, and -9 and TIMP-2 in tracheal aspirates from preterm infants with respiratory distress. Pediatrics 2001;108:686-692.
30. Lanone S, Zheng T, Zhu Z, Liu W, Lee CG, Ma B, Chen Q, Homer RJ, Wang J, Rabach LA, et al. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J Clin Invest 2002;110:463-474. (Pubitemid 34919700)
31. Coalson JJ, Winter VT, Siler-Khodr T, Yoder BA. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med 1999;160:1333-1346. (Pubitemid 29487478)
32. McCurnin DC, Pierce RA, Chang LY, Gibson LL, Osborne-Lawrence S, Yoder BA, Kerecman JD, Albertine KH, Winter VT, Coalson JJ, et al. Inhaled NO improves early pulmonary function and modifies lung growth and elastin deposition in a baboon model of neonatal chronic lung disease. Am J Physiol Lung Cell Mol Physiol 2005;288: L450-L459. (Pubitemid 40229510)
33. Coalson JJ, Winter VT, Gerstmann DR, Idell S, King RJ, Delemos RA. Pathophysiologic, morphometric, and biochemical studies of the premature baboon with bronchopulmonary dysplasia. Am Rev Respir Dis 1992;145:872-881.
34. Yasumatsu R, Altiok O, Benarafa C, Yasumatsu C, Bingol-Karakoc G, Remold-O'Donnell E, Cataltepe S. SERPINB1 upregulation is associated with in vivo complex formation with neutrophil elastase and cathepsin G in a baboon model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2006;291:L619-L627. (Pubitemid 44498472)
35. Altiok O, Yasumatsu R, Bingol-Karakoc G, Riese RJ, StahlmanMT, Dwyer W, Pierce RA, Bromme D, Weber E, Cataltepe S. Imbalance between cysteine proteases and inhibitors in a baboon model of bronchopulmonary dysplasia. Am J Respir Crit Care Med 2006;173:318-326. (Pubitemid 43209087)
36. Bhandari V, Choo-Wing R, Lee CG, Zhu Z, Nedrelow JH, Chupp GL, Zhang X, Matthay MA, Ware LB, Homer RJ, et al. Hyperoxia causes angiopoietin 2-mediated acute lung injury and necrotic cell death. Nat Med 2006;12:1286-1293. (Pubitemid 44706931)
37. Aghai ZH, Faqiri S, Saslow JG, Nakhla T, Farhath S, Kumar A, Eydelman R, Strande L, Stahl G, Leone P, et al. Angiopoietin 2 concentrations in infants developing bronchopulmonary dysplasia: attenuation by dexamethasone. J Perinatol 2008;28:149-155. (Pubitemid 351217643)
38. Rishikof DC, Lucey EC, Kuang PP, Snider GL, Goldstein RH. Induction of the myofibroblast phenotype following elastolytic injury to mouse lung. Histochem Cell Biol 2006;125:527-534. (Pubitemid 43673515)
39. Mauad T, Hajjar LA, Callegari GD, da Silva LF, Schout D, Galas FR, Alves VA, Malheiros DM, Auler Jr JO, Ferreira AF, et al. Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 2010;181:72-79.
40. Zheng T, Kang MJ, Crothers K, Zhu Z, Liu W, Lee CG, Rabach LA, Chapman HA, Homer RJ, Aldous D, et al. Role of cathepsin S- dependent epithelial cell apoptosis in IFN-gamma-induced alveolar remodeling and pulmonary emphysema. J Immunol 2005;174:8106-8115. (Pubitemid 40806322)
41. Bhandari V, Choo-Wing R, Lee CG, Yusuf K, Nedrelow JH, Ambalavanan N, Malkus H, Homer RJ, Elias JA. Developmental regulation of NO-mediated VEGF-induced effects in the lung. Am J Respir Cell Mol Biol 2008;39:420-430.
42. Choo-Wing R, Nedrelow JH, Homer RJ, Elias JA, Bhandari V. Developmental differences in the responses of IL-6 and IL-13 transgenic mice exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 2007;293:L142-L150. (Pubitemid 47080722)
43. Bhandari V, Elias JA. Cytokines in tolerance to hyperoxia-induced injury in the developing and adult lung. Free Radic Biol Med 2006;41:4-18. (Pubitemid 43866449)
44. Yang G, Abate A, George AG, Weng YH, Dennery PA. Maturational differences in lung NF-kappaB activation and their role in tolerance to hyperoxia. J Clin Invest 2004;114:669-678. (Pubitemid 39578757)
45. Ambalavanan N, Carlo WA, D'Angio CT, McDonald SA, Das A, Schendel D, Thorsen P, Higgins RD. Cytokines associated with bronchopulmonary dysplasia or death in extremely low birth weight infants. Pediatrics 2009;123:1132-1141.
46. Dik WA, van Kaam AH, Dekker T, Naber BA, Janssen DJ, Kroon AA, Zimmermann LJ, Versnel MA, Lutter R. Early increased levels of matrix metalloproteinase-9 in neonates recovering from respiratory distress syndrome. Biol Neonate 2006;89:6-14. (Pubitemid 43087503)
47. Pardo A, Barrios R, Maldonado V, Melendez J, Perez J, Ruiz V, Segura- Valdez L, Sznajder JI, Selman M. Gelatinases A and B are up-regulated in rat lungs by subacute hyperoxia: pathogenetic implications. Am J Pathol 1998;153:833-844. (Pubitemid 28419036)
48. Devaskar UP, Taylor W, Govindrajan R, Malicdem M, Heyman S, deMello DE. Hyperoxia induces interstitial (Type I) and increases Type IV collagenase mRNA expression and increases Type I and IV collagenolytic activity in newborn rat lung. Biol Neonate 1994; 66:76-85.
49. Radomski A, Sawicki G, Olson DM, Radomski MW. The role of nitric oxide and metalloproteinases in the pathogenesis of hyperoxia-induced lung injury in newborn rats. Br J Pharmacol 1998;125:1455-1462. (Pubitemid 28548557)
50. Kraling BM, Wiederschain DG, Boehm T, Rehn M, Mulliken JB, Moses MA. The role of matrix metalloproteinase activity in the maturation of human capillary endothelial cells in vitro. J Cell Sci 1999;112:1599-1609. (Pubitemid 29261321)
51. Sweet DG, Curley AE, Chesshyre E, Pizzotti J, Wilbourn MS, Halliday HL, Warner JA. The role of matrix metalloproteinases-9 and -2 in development of neonatal chronic lung disease. Acta Paediatr 2004;93: 791-796. (Pubitemid 38736814)
52. Lukkarinen H, Hogmalm A, Lappalainen U, Bry K. Matrix metalloproteinase- 9 deficiency worsens lung injury in a model of bronchopulmonary dysplasia. Am J Respir Cell Mol Biol 2009;41:59-68.
53. Tambunting F, Beharry KD, Hartleroad J, Waltzman J, Stavitsky Y, Modanlou HD. Increased lung matrix metalloproteinase-9 levels in extremely premature baboons with bronchopulmonary dysplasia. Pediatr Pulmonol 2005;39:5-14. (Pubitemid 39628597)
54. Kallapur SG, Jobe AH, Ikegami M, Bachurski CJ. Increased IP-10 and MIG expression after intra-amniotic endotoxin in preterm lamb lung. Am J Respir Crit Care Med 2003;167:779-786. (Pubitemid 36801758)
55. Bourbon JR, Boucherat O, Boczkowski J, Crestani B, Delacourt C. Bronchopulmonary dysplasia and emphysema: in search of common therapeutic targets. Trends Mol Med 2009;15:169-179.