Inhibition of apoptosis by 60% oxygen: A novel pathway contributing to lung injury in neonatal rats

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 3, 2011, Pages

  Yi, Man ^a   Masood, Azhar ^a,b   Ziino, Adrian ^a,b,c   Johnson, Ben Hur ^a,b   Belcastro, Rosetta ^a   Li, Jun ^a   Shek, Samuel ^a   Kantores, Crystal ^c   Jankov, Robert P ^b,c   Keith Tanswell, A ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Canada   (Canada)

Author keywords

Bronchopulmonary dysplasia; Chronic neonatal lung injury; Survivin

Indexed keywords

CASPASE 3; CASPASE 7; CYTOCHROME C; OXYGEN; PROTEIN BAX; PROTEIN BCL XL; SURVIVIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL GROWTH; CELL PROLIFERATION; DNA FRAGMENTATION; ENZYME ACTIVITY; FEMALE; HYPEROXIA; IMMUNOHISTOCHEMISTRY; LUNG ALVEOLUS CELL; LUNG DEVELOPMENT; LUNG INJURY; NEWBORN; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AIR; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CELL COUNT; CELL DEATH; FEMALE; IMMUNOHISTOCHEMISTRY; LUNG; LUNG INJURY; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STAUROSPORINE;

EID: 79955029898     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00126.2010     Document Type: Article

References (64)

1. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326, 1998.
2. Adida C, Crotty PL, McGrath J, Berrebi D, Diebold J, Altieri DC. Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am J Pathol 152: 43-49, 1998.
3. Ahola T, Fellman V, Kjellmer I, Raivio KO, Lapatto R. Plasma 8-isoprostane is increased in preterm infants who develop bronchopulmo-nary dysplasia or periventricular leukomalacia. Pediatr Res 56: 88-93, 2004.
4. Albertine KH, Jones GP, Starcher BC, Bohnsack JF, Davis PL, Cho SC, Carlton DP, Bland RD. Chronic lung injury in preterm lambs. Am J Respir Crit Care Med 159: 945-958, 1999.
5. Allen RT, Cluck MW, Agrawal DK. Mechanisms controlling cellular suicide: role of Bcl-2 and caspases. Cell Mol Life Sci 54: 427-445, 1998.
6. Altieri DC, Marchisio PC. Survivin apoptosis: an interloper between cell death and cell proliferation in cancer. Lab Invest 79: 1327-1333, 1999.
7. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3: 46-54, 2003.
8. Ambalavanan N, Novak ZE. Peptide growth factors in tracheal aspirates of mechanically ventilated preterm neonates. Pediatr Res 53: 240-244, 2003.
9. Banks BA, Ischiropoulos H, McClelland M, Ballard PL, Ballard RA. Plasma 3-nitrotyrosine is elevated in premature infants who develop bronchopulmonary dysplasia. Pediatrics 101: 870-874, 1998.
10. Been JV, Debeer A, van Iwaarden JF, Kloosterboer N, Passos VL, Naulaers G, Zimmermann LJ. Early alterations of growth factor patterns in bronchoalveolar lavage fluid from preterm infants developing broncho-pulmonary dysplasia. Pediatr Res 67: 83-89, 2010.
11. Bhandari V, Choo-Wing R, Lee CG, Zhu Z, Nedrelow JH, Chupp GL, Zhang X, Matthay MA, Ware LB, Homer RJ, Lee PJ, Geick A, de Fougerolles AR, Elias JA. Hyperoxia causes angiopoietin 2-mediated acute lung injury and necrotic cell death. Nat Med 12: 1286-1293, 2006.
12. Blanc-Brude OP, Yu J, Simosa H, Conte MS, Sessa WC, Altieri DC. Inhibitor of apoptosis protein survivin regulates vascular injury. Nat Med 8: 987-994, 2002.
13. Buch S, Han RN, Cabacungan J, Wang J, Yuan S, Belcastro R, Deimling J, Jankov R, Luo X, Lye SJ, Post M, Tanswell AK. Changes in expression of platelet-derived growth factor and its receptors in the lungs of newborn rats exposed to air or 60% O2. Pediatr Res 48: 423-433, 2000.
14. Burri PH. Structural aspects of prenatal and postnatal development and growth of the lung. In: Lung Growth and Development, edited by McDonald JA. New York: Dekker, 1997, p. 1-35.
15. Caporossi D, Ciafrè SA, Pittaluga M, Savini I, Farace MG. Cellular responses to H2O2 and bleomycin-induced oxidative stress in L6C5 rat myoblasts. Free Radic Biol Med 35: 1355-1364, 2003.
16. 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 145: 872-881, 1992.
17. Coalson JJ. Pathology of chronic lung disease of early infancy. In: Chronic Lung Disease in Early Infancy, edited by Bland RD and Coalson JJ. New York: Dekker, 2000, p. 85-124.
18. Cutz E, Chaisson D. Chronic lung disease after premature birth. N Engl J Med 358: 743-746, 2008.
19. Dieperink HI, Blackwell TS, Prince LS. Hyperoxia and apoptosis in developing mouse lung mesenchyme. Pediatr Res 59: 185-190, 2006.
20. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383-424, 1999.
21. Franco-Montoya ML, Bourbon JR, Durrmeyer X, Lorotte S, Jarreau PH, Delacourt C. Pulmonary effects of keratinocyte growth factor in newborn rats exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 297: L965-L976, 2009.
22. Han RN, Buch S, Tseu I, Young J, Christie NA, Frndova H, Lye SJ, Post M, Tanswell AK. Changes in structure, mechanics, and insulin-like growth factor-related gene expression in the lungs of newborn rats exposed to air or 60% oxygen. Pediatr Res 39: 921-929, 1996.
23. He CH, Waxman AB, Lee CG, Link H, Rabach ME, Ma B, Chen Q, Zhu Z, Zhong M, Nakayama K, Nakayama KI, Homer R, Elias JA. Bcl-2-related protein A1 is an endogenous and cytokine-stimulated mediator of cytoprotection in hyperoxic acute lung injury. J Clin Invest 115: 1039-1048, 2005.
24. Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577-580, 1981.
25. Husari AW, Dbaibo GS, Bitar H, Khayat A, Panjarian S, Nasser M, Bitar FF, El-Sabban M, Zaatari G, Mroueh SM. Apoptosis and the activity of ceramide, Bax and Bcl-2 in the lungs of neonatal rats exposed to limited and prolonged hyperoxia. Respir Res 7: 100, 2006.
26. Ireys HT, Anderson GF, Shaffer TJ, Neff JM. Expenditures for care of children with chronic illnesses enrolled in the Washington State Medical Program, fiscal year 1993. Pediatrics 100: 197-204, 1997.
27. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279: L600-L607, 2000.
28. Jankov RP, Luo X, Cabacungan J, Belcastro R, Frndova H, Lye SJ, Tanswell AK. Endothelin-1 and O2-mediated pulmonary hypertension in neonatal rats: a role for products of lipid peroxidation. Pediatr Res 48: 289-298, 2000.
29. Jankov RP, Luo X, Belcastro R, Copland I, Frndova H, Lye SJ, Hoidal JR, Post M, Tanswell AK. Gadolinium chloride inhibits pulmonary macrophage influx and prevents O2-induced pulmonary hypertension in the neonatal rat. Pediatr Res 50: 172-183, 2001.
30. Jankov RP, Luo X, Campbell A, Belcastro R, Cabacungan J, John-stone L, Frndova H, Lye SJ, Tanswell AK. Fibroblast growth factor receptor-1 and compensatory neonatal lung growth after 95% oxygen exposure. Am J Respir Crit Care Med 167: 1554-1561, 2003.
31. Jin Z, El-Deiry WS. Overview of cell death signaling pathways. Cancer Biol Ther 4: 139-163, 2005.
32. Johnson BH, Yi M, Masood A, Belcastro R, Shek S, Kantores C, Jankov RP, Tanswell AK. A critical role for interleukin-1 receptor in the lung injury induced in neonatal rats by 60% oxygen. Pediatr Res 66: 260-265, 2009.
33. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 106: 1311-1319, 2002.
34. Knauer SK, Mann W, Stauber RH. Survivin's dual role: an export's view. Cell Cycle 6: 518-521, 2007.
35. Lakhani SA, Masud A, Kuida K, Porter GA Jr, Booth CJ, Mehal WZ, Inayat I, Flavell RA. Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311: 847-851, 2006.
36. Lassus P, Heikkilä P, Andersson LC, Boguslawski K, Andersson S. Lower concentration of pulmonary hepatocyte growth factor is associated with more severe lung disease in preterm infants. J Pediatr 143: 199-202, 2003.
37. Lau A, Arundine M, Sun HS, Jones M, Tymianski M. Inhibition of caspase-mediated apoptosis by peroxynitrite in traumatic brain injury. J Neurosci 26: 11540-11553, 2006.
38. Len SM, Vader G, Medema RH. The case for Survivin as mitotic regulator. Curr Opin Cell Biol 18: 616-622, 2006.
39. Lindahl P, Karlsson L, Hellstrom M, Gebre-Medhin S, Willetts K, Heath JK, Betsholtz C. Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development. Development 124: 3943-3953, 1997.
40. Luo X, Christie NA, McLaughlin MA, Belcastro R, Sedlackova L, Cabacungan J, Freeman BA, Tanswell AK. H2O2 mediates O2 toxicity in cultured fetal rat distal lung epithelial cells. Free Radic Biol Med 26: 1357-1368, 1999.
41. Maniscalco WM, Watkins RH, O'Reilly MA, Shea CP. Increased epithelial cell proliferation in very premature baboons with chronic lung disease. Am J Physiol Lung Cell Mol Physiol 283: L991-L1001, 2002.
42. Masood A, Yi M, Lau M, Belcastro R, Shek S, Pan J, Kantores C, McNamara PJ, Kavanagh BP, Belik J, Jankov RP, Tanswell AK. Therapeutic effects of hypercapnia on chronic lung injury and vascular remodeling in neonatal rats. Am J Physiol Lung Cell Mol Physiol 297: L920-L930, 2009.
43. Masood A, Belcastro R, Li J, Kantores C, Jankov RP, Tanswell AK. A peroxynitrite decomposition catalyst prevents 60% O2-mediated rat chronic neonatal lung injury. Free Radic Biol Med 49: 1182-1191, 2010.
44. McMurtry MS, Archer SL, Altieri DC, Bonnet S, Haromy A, Harry G, Bonnet S, Puttagunta L, Michelakis ED. Gene therapy targeting survivin selectively induces pulmonary vascular apoptosis and reverses pulmonary arterial hypertension. J Clin Invest 115: 1479-1491, 2005.
45. Meyrick B, Reid L. Pulmonary arterial and alveolar development in normal postnatal rat lung. Am Rev Respir Dis 125: 468-473, 1982.
46. Murphy PR, Limoges M, Dodd F, Boudreau RTM, Too CKL. Fibroblast growth factor-2 stimulates endothelial nitric oxide synthase expression and inhibits apoptosis by a nitric oxide-dependent pathway in Nb2 lymphoma cells. Endocrinology 142: 81-88, 2001.
47. Niu JO, Munshi UK, Siddiq MM, Parton LA. Early increase in endothelin-1 in tracheal aspirates of preterm infants: correlation with bronchopulmonary dysplasia. J Pediatr 132: 965-970, 1998.
48. O'Connor DS, Schechner JS, Adida C, Mesri M, Rothermel AL, Li F, Nath AK, Pober JS, Altieri DC. Control of apoptosis during angiogen-esis by survivin expression in endothelial cells. Am J Pathol 156: 393-398, 2000.
49. Padela S, Cabacungan J, Shek S, Belcastro R, Yi M, Jankov RP, Tanswell AK. Hepatocyte growth factor is required for alveologenesis in the neonatal rat. Am J Respir Crit Care Med 172: 907-914, 2005.
50. Padela S, Yi M, Cabacungan J, Shek S, Belcastro R, Masood A, Jankov RP, Tanswell AK. A critical role for fibroblast growth factor-7 during early alveolar formation in the neonatal rat. Pediatr Res 63: 232-238, 2008.
51. Sano H, Ueda Y, Takakura N, Takemura G, Doi T, Kataoka H, Murayama T, Xu Y, Sudo T, Nishikawa S, Fujiwara H, Kita T, Yokode M. Blockade of platelet-derived growth factor receptor- fj pathway induces apoptosis of vascular endothelial cells and disrupts glomerular capillary formation in neonatal mice. Am J Pathol 161: 135-143, 2002.
52. Scavo LM, Ertsey R, Chapin CJ, Allen L, Kitterman JA. Apoptosis in the development of rat and human fetal lungs. Am J Respir Cell Mol Biol 18: 21-31, 1998.
53. Schittny JC, Djonov V, Fine A, Burri PH. Programmed cell death contributes to postnatal lung development. Am J Respir Cell Mol Biol 18: 786-793, 1998.
54. Sunday ME, Yoder BA, Cuttitta F, Haley KJ, Emanuel RL. Bombesin-like peptide mediates lung injury in a baboon model of bronchopulmonary dysplasia. J Clin Invest 102: 584-594, 1998.
55. Takeuchi H, Kim J, Fujimoto A, Umetani N, Mori T, Bilchik A, Turner R, Tran A, Kuo C, Hoon DS. X-Linked inhibitor of apoptosis protein expression level in colorectal cancer is regulated by hepatocyte growth factor/C-met pathway via Akt signaling. Clin Cancer Res 11: 7621-7628, 2005.
56. Tanswell AK, Joneja MG, Lindsay J, Vreeken E. Differentiation-arrested rat fetal lung in primary monolayer cell culture. I. Development of a differentiation-arrested and growth-supporting culture system using carbon-stripped bovine fetal calf serum. Exp Lung Res 5: 37-48, 1983.
57. Tanswell AK, Fraher LJ, Grose EC. Circulating factors that modify lung cell DNA synthesis following exposure to inhaled oxidants. I. Effect of serum and lavage on lung fibroblasts following exposure of adult rats to 1 ppm ozone. J Toxicol Environ Health 27: 239-254, 1989.
58. Tanswell AK, Padela S, Jankov RP. Altered growth factor signaling in the pathogenesis of BPD. In: Bronchopulmonary Dysplasia, edited by Abman SH. New York: Informa, 2009, p. 188-207.
59. Wang X, Zhou YS, Kim HP, Song RP, Zarnegar R, Ryter SW, Choi AMK. Hepatocyte growth factor protects against hypoxia/reoxygenation-induced apoptosis in endothelial cells. J Biol Chem 279: 5237-5243, 2004.
60. Warner BB, Stuart LA, Papes RA, Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol Lung Cell Mol Physiol 275: L110-L117, 1998.
61. Wong PM, Lees AN, Louw J, Lee FY, French N, Gain K, Murray CP, Wilson A, Chambers DC. Emphysema in young adult survivors of moderate-to-severe bronchopulmonary dysplasia. Eur Respir J 32: 321-328, 2008.
62. Yi M, Jankov RP, Belcastro R, Humes D, Copland I, Shek S, Sweezey NB, Post M, Albertine KH, Auten RL, Tanswell AK. Opposing effects of 60% oxygen and neutrophil influx on alveologenesis in the neonatal rat. Am J Respir Crit Care Med 170: 1188-1196, 2004.
63. Yi M, Belcastro R, Shek S, Luo D, Post M, Tanswell AK. Fibroblast growth factor-2 and receptor-1alpha(IIIc) regulate postnatal rat lung cell apoptosis. Am J Respir Crit Care Med 174: 581-589, 2006.
64. Zhang M, Lin L, Lee SJ, Mo L, Cao J, Ifedigbo E, Jin Y. Deletion of caveolin-1 protects hyperoxia-induced apoptosis via survivin-medi-ated pathways. Am J Physiol Lung Cell Mol Physiol 297: L945-L953, 2009.