The role of hyperoxia in the pathogenesis of experimental BPD

Seminars in Perinatology

Volumn 37, Issue 2, 2013, Pages 69-78

  Buczynski, Bradley W ^a   Maduekwe, Echezona T ^a   O'Reilly, Michael A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Bronchopulmonary dysplasia; Hyperoxia; Lung development

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; VASCULOTROPIN;

ATMOSPHERIC PRESSURE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; ENVIRONMENTAL STRESS; EXPERIMENTAL STUDY; GENE EXPRESSION REGULATION; GENE INTERACTION; HUMAN; HYPEROXIA; HYPOXIA INDUCIBLE FACTOR 1ALPHA GENE; HYPOXIA INDUCIBLE FACTOR 1BETA GENE; HYPOXIA INDUCIBLE FACTOR 2ALPHA GENE; LONG TERM EXPOSURE; LUNG DEVELOPMENT; LUNG DYSPLASIA; NEWBORN CARE; NONHUMAN; OXYGEN THERAPY; OXYGEN TOXICITY; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VASCULOTROPIN GENE;

ANIMALS; ANIMALS, NEWBORN; BRONCHOPULMONARY DYSPLASIA; DISEASE MODELS, ANIMAL; GENE-ENVIRONMENT INTERACTION; HUMANS; HYPEROXIA; INFANT, NEWBORN; INFANT, PREMATURE; LUNG; OXIDATIVE STRESS; OXYGEN INHALATION THERAPY; RESPIRATION, ARTIFICIAL;

EID: 84876118849     PISSN: 01460005     EISSN: 1558075X     Source Type: Journal    
DOI: 10.1053/j.semperi.2013.01.002     Document Type: Review

References (130)

1. March of Dimes P, Save the Children, WHO. Born Too Soon: The Global Action Report on Preterm Birth 2012, World Health Organization, Geneva. C.P. Howson, M.V. Kinney, J.E. Lawn (Eds.).
2. Jobe A.H., Kallapur S.G. Long term consequences of oxygen therapy in the neonatal period. Semin Fetal Neonatal Med 2010, 15(4):230-235.
3. Smith V.C., Zupancic J.A., McCormick M.C., et al. Rehospitalization in the first year of life among infants with bronchopulmonary dysplasia. J Pediatr 2004, 144(6):799-803.
4. Jobe A.H., Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001, 163(7):1723-1729.
5. Baraldi E., Filippone M. Chronic lung disease after premature birth. N Engl J Med 2007, 357(19):1946-1955.
6. Chess P.R., D'Angio C.T., Pryhuber G.S., Maniscalco W.M. Pathogenesis of bronchopulmonary dysplasia. Semin Perinatol 2006, 30(4):171-178.
7. Northway W.H., Rosan R.C. Radiographic features of pulmonary oxygen toxicity in the newborn: bronchopulmonary dysplasia. Radiology 1968, 91(1):49-58.
8. Saigal S., O'Brodovich H. Long-term outcome of preterm infants with respiratory disease. Clin Perinatol 1987, 14(3):635-650.
9. Northway W.H., Moss R.B., Carlisle K.B., et al. Late pulmonary sequelae of bronchopulmonary dysplasia. N Engl J Med 1990, 323(26):1793-1799.
10. Saigal S., Doyle L.W. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008, 371(9608):261-269.
11. Doyle L.W., Faber B., Callanan C., Morley R. Blood pressure in late adolescence and very low birth weight. Pediatrics 2003, 111(2):252-257.
12. Ward R.M., Beachy J.C. Neonatal complications following preterm birth. Br J Obstet Gynecol 2003, 110(suppl. 20):8-16.
13. Northway W.H., Rosan R.C., Porter D.Y. Pulmonary disease following respirator therapy of hyaline-membrane disease. Bronchopulmonary dysplasia. N Engl J Med 1967, 276(7):357-368.
14. Jobe A.J. The new BPD: an arrest of lung development. Pediatr Res 1999, 46(6):641-643.
15. Abman S.H. Bronchopulmonary dysplasia: "a vascular hypothesis". Am J Respir Crit Care Med 2001, 164(10 Pt 1):1755-1756.
16. Kair L.R., Leonard D.T., Anderson J.M. Bronchopulmonary dysplasia. Pediatr Rev 2012, 33(6):255-263. [quiz 63-4].
17. Bonikos D.S., Bensch K.G., Northway W.H. Oxygen toxicity in the newborn. The effect of chronic continuous 100 percent oxygen exposure on the lungs of newborn mice. Am J Pathol 1976, 85(3):623-650.
18. Coalson J.J., Winter V.T., Siler-Khodr T., Yoder B.A. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med 1999, 160(4):1333-1346.
19. Barker D.J., Winter P.D., Osmond C., Margetts B., Simmonds S.J. Weight in infancy and death from ischaemic heart disease. Lancet 1989, 2(8663):577-580.
20. Berner R.A., Vandenbrooks J.M., Ward P.D. Evolution. Oxygen and evolution. Science 2007, 316(5824):557-558.
21. Fluck M., Webster K.A., Graham J., Giomi F., Gerlach F., Schmitz A. Coping with cyclic oxygen availability: evolutionary aspects. Integr Comp Biol 2007, 47(4):524-531.
22. Stamati K., Mudera V., Cheema U. Evolution of oxygen utilization in multicellular organisms and implications for cell signalling in tissue engineering. J Tissue Eng 2011, 2(1). [2041731411432365].
23. Thannickal V.J. Oxygen in the evolution of complex life and the price we pay. Am J Respir Cell Mol Biol 2009, 40(5):507-510.
24. Frazier M.R., Woods H.A., Harrison J.F. Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiol Biochem Zool 2001, 74(5):641-650.
25. Taylor C.T., McElwain J.C. Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans. Physiology (Bethesda) 2010, 25(5):272-279.
26. Ratcliffe P.J., O'Rourke J.F., Maxwell P.H., Pugh C.W. Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J Exp Biol 1998, 201(Pt 8):1153-1162.
27. Taylor C.T. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J 2008, 409(1):19-26.
28. Semenza G.L. Life with oxygen. Science. 5 2007, 318(847):62-64.
29. Semenza G.L. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007, 2007(407). cm8.
30. Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004, 5(5):343-354.
31. Groenman F., Rutter M., Caniggia I., Tibboel D., Post M. Hypoxia-inducible factors in the first trimester human lung. J Histochem Cytochem 2007, 55(4):355-363.
32. Compernolle V., Brusselmans K., Franco D., et al. Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1alpha. Cardiovasc Res 2003, 60(3):569-579.
33. Brusselmans K., Compernolle V., Tjwa M., et al. Heterozygous deficiency of hypoxia-inducible factor-2alpha protects mice against pulmonary hypertension and right ventricular dysfunction during prolonged hypoxia. J Clin Invest 2003, 111(10):1519-1527.
34. Asikainen T.M., Chang L.Y., Coalson J.J., et al. Improved lung growth and function through hypoxia-inducible factor in primate chronic lung disease of prematurity. FASEB J 2006, 20(10):1698-1700.
35. Asikainen T.M., Waleh N.S., Schneider B.K., Clyman R.I., White C.W. Enhancement of angiogenic effectors through hypoxia-inducible factor in preterm primate lung in vivo. Am J Physiol Lung Cell Mol Physiol 2006, 291(4):L588-L595.
36. Stenmark K.R., Abman S.H. Lung vascular development: implications for the pathogenesis of bronchopulmonary dysplasia. Annu Rev Physiol 2005, 67:623-661.
37. Carmeliet P., Ferreira V., Breier G., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380(6573):435-439.
38. Maniscalco W.M., Watkins R.H., D'Angio C.T., Ryan R.M. Hyperoxic injury decreases alveolar epithelial cell expression of vascular endothelial growth factor (VEGF) in neonatal rabbit lung. Am J Respir Cell Mol Biol 1997, 16(5):557-567.
39. Lin Y.J., Markham N.E., Balasubramaniam V., et al. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr Res 2005, 58(1):22-29.
40. Balasubramaniam V., Mervis C.F., Maxey A.M., Markham N.E., Abman S.H. Hyperoxia reduces bone marrow, circulating, and lung endothelial progenitor cells in the developing lung: implications for the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2007, 292(5):L1073-L1084.
41. Maniscalco W.M., Watkins R.H., Roper J.M., Staversky R., O'Reilly M.A. Hyperoxic ventilated premature baboons have increased p53, oxidant DNA damage and decreased VEGF expression. Pediatr Res 2005, 58(3):549-556.
42. Hosford G.E., Olson D.M. Effects of hyperoxia on VEGF, its receptors, and HIF-2alpha in the newborn rat lung. Am J Physiol Lung Cell Mol Physiol 2003, 285(1):L161-L168.
43. Watkins R.H., D'Angio C.T., Ryan R.M., Patel A., Maniscalco W.M. Differential expression of VEGF mRNA splice variants in newborn and adult hyperoxic lung injury. Am J Physiol 1999, 276(5 Pt 1):L858-L867.
44. Asikainen T.M., Ahmad A., Schneider B.K., White C.W. Effect of preterm birth on hypoxia-inducible factors and vascular endothelial growth factor in primate lungs. Pediatr Pulmonol 2005, 40(6):538-546.
45. Meller S., Bhandari V. VEGF levels in humans and animal models with RDS and BPD: temporal relationships. Exp Lung Res 2012, 38:192-203.
46. Bhatt A.J., Pryhuber G.S., Huyck H., Watkins R.H., Metlay L.A., Maniscalco W.M. Disrupted pulmonary vasculature and decreased vascular endothelial growth factor, Flt-1, and TIE-2 in human infants dying with bronchopulmonary dysplasia. Am J Respir Crit Care Med. 164 2001, 10 Pt 1:1971-1980.
47. Bhandari V., Choo-Wing R., Lee C.G., et al. Developmental regulation of NO-mediated VEGF-induced effects in the lung. Am J Respir Cell Mol Biol 2008, 39(4):420-430.
48. D'Angio C.T., Maniscalco W.M. The role of vascular growth factors in hyperoxia-induced injury to the developing lung. Front Biosci 2002, 7:d1609-d1623.
49. Smith L.J., McKay K.O., van Asperen P.P., Selvadurai H., Fitzgerald D.A. Normal development of the lung and premature birth. Paediatr Respir Rev 2010, 11(3):135-142.
50. Mendelson C.R. Role of transcription factors in fetal lung development and surfactant protein gene expression. Annu Rev Physiol 2000, 62:875-915.
51. Sola A., Rogido M.R., Deulofeut R. Oxygen as a neonatal health hazard: call for detente in clinical practice. Acta Paediatr 2007, 96(6):801-812.
52. Supplemental Therapeutic Oxygen for Prethreshold Retinopathy Of Prematurity (STOP-ROP), a randomized, controlled trial. I: primary outcomes. Pediatrics 2000, 105(2):295-310.
53. Askie L.M., Henderson-Smart D.J., Irwig L., Simpson J.M. Oxygen-saturation targets and outcomes in extremely preterm infants. N Engl J Med 2003, 349(10):959-967.
54. Tin W., Milligan D.W., Pennefather P., Hey E. Pulse oximetry, severe retinopathy, and outcome at one year in babies of less than 28 weeks gestation. Arch Dis Child Fetal Neonatal Ed 2001, 84(2):F106-F110.
55. Deulofeut R., Critz A., Adams-Chapman I., Sola A. Avoiding hyperoxia in infants < or = 1250g is associated with improved short- and long-term outcomes. J Perinatol 2006, 26(11):700-705.
56. Carlo W.A., Finer N.N., Walsh M.C., et al. Target ranges of oxygen saturation in extremely preterm infants. N Engl J Med 2010, 362(21):1959-1969.
57. Finer N.N., Carlo W.A., Walsh M.C., et al. Early CPAP versus surfactant in extremely preterm infants. N Engl J Med 2010, 362(21):1970-1979.
58. Stevens T.P., Dylag A., Panthagani I., Pryhuber G., Halterman J. Effect of cumulative oxygen exposure on respiratory symptoms during infancy among VLBW infants without bronchopulmonary dysplasia. Pediatr Pulmonol 2010, 45(4):371-379.
59. Wright C.J., Dennery P.A. Manipulation of gene expression by oxygen: a primer from bedside to bench. Pediatr Res 2009, 66(1):3-10.
60. Frank L., Bucher J.R., Roberts R.J. Oxygen toxicity in neonatal and adult animals of various species. J Appl Physiol 1978, 45(5):699-704.
61. Clark J.M., Lambertsen C.J. Pulmonary oxygen toxicity: a review. Pharmacol Rev 1971, 23(2):37-133.
62. Robinson F.R., Casey H.W., Weibel E.R. Animal model: oxygen toxicity in nonhuman primates. Am J Pathol 1974, 76(1):175-178.
63. Frank L. Developmental aspects of experimental pulmonary oxygen toxicity. Free Radic Biol Med 1991, 11(5):463-494.
64. Johnston C.J., Wright T.W., Reed C.K., Finkelstein J.N. Comparison of adult and newborn pulmonary cytokine mRNA expression after hyperoxia. Exp Lung Res 1997, 23(6):537-552.
65. D'Angio C.T., Johnston C.J., Wright T.W., Reed C.K., Finkelstein J.N. Chemokine mRNA alterations in newborn and adult mouse lung during acute hyperoxia. Exp Lung Res 1998, 24(5):685-702.
66. Wilborn A.M., Evers L.B., Canada A.T. Oxygen toxicity to the developing lung of the mouse: role of reactive oxygen species. Pediatr Res 1996, 40(2):225-232.
67. Weinberger B., Laskin D.L., Heck D.E., Laskin J.D. Oxygen toxicity in premature infants. Toxicol Appl Pharmacol 2002, 181(1):60-67.
68. Saugstad O.D. Oxygen and oxidative stress in bronchopulmonary dysplasia. J Perinat Med 2010, 38(6):571-577.
69. Vento M., Escobar J., Cernada M., Escrig R., Aguar M. The use and misuse of oxygen during the neonatal period. Clin Perinatol 2012, 39(1):165-176.
70. Collard K.J., Godeck S., Holley J.E., Quinn M.W. Pulmonary antioxidant concentrations and oxidative damage in ventilated premature babies. Arch Dis Child Fetal Neonatal Ed 2004, 89(5):F412-F416.
71. Gladstone I.M., Levine R.L. Oxidation of proteins in neonatal lungs. Pediatrics 1994, 93(5):764-768.
72. Smith C.V., Hansen T.N., Martin N.E., McMicken H.W., Elliott S.J. Oxidant stress responses in premature infants during exposure to hyperoxia. Pediatr Res 1993, 34(3):360-365.
73. Auten R.L., O'Reilly M.A., Oury T.D., Nozik-Grayck E., Whorton M.H. Transgenic extracellular superoxide dismutase protects postnatal alveolar epithelial proliferation and development during hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006, 290(1):L32-L40.
74. Wispe J.R., Warner B.B., Clark J.C., et al. Human Mn-superoxide dismutase in pulmonary epithelial cells of transgenic mice confers protection from oxygen injury. J Biol Chem 1992, 267(33):23937-23941.
75. Coates A.L., Desmond K., Willis D., Nogrady M.B. Oxygen therapy and long-term pulmonary outcome of respiratory distress syndrome in newborns. Am J Dis Child 1982, 136(10):892-895.
76. Kennedy J.D., Edward L.J., Bates D.J., et al. Effects of birthweight and oxygen supplementation on lung function in late childhood in children of very low birth weight. Pediatr Pulmonol 2000, 30(1):32-40.
77. Davis J.M., Parad R.B., Michele T., Allred E., Price A., Rosenfeld W. Pulmonary outcome at 1 year corrected age in premature infants treated at birth with recombinant human CuZn superoxide dismutase. Pediatrics 2003, 111(3):469-476.
78. Parad R.B., Allred E.N., Rosenfeld W.N., Davis J.M. Reduction of retinopathy of prematurity in extremely low gestational age newborns treated with recombinant human Cu/Zn superoxide dismutase. Neonatology 2012, 102(2):139-144.
79. Sosenko I.R., Frank L. Nutritional influences on lung development and protection against chronic lung disease. Semin Perinatol 1991, 15(6):462-468.
80. 2 toxicity. Pediatr Res 1985, 19(3):281-286.
81. Frank L., Roberts R.J. Effects of low-dose prenatal corticosteroid administration on the premature rat. Biol Neonate 1979, 36(1-2):1-9.
82. Walther F.J., Jobe A.H., Ikegami M. Repetitive prenatal glucocorticoid therapy reduces oxidative stress in the lungs of preterm lambs. J Appl Physiol 1998, 85(1):273-278.
83. Vento M., Aguar M., Escobar J., et al. Antenatal steroids and antioxidant enzyme activity in preterm infants: influence of gender and timing. Antioxid Redox Signal 2009, 11(12):2945-2955.
84. Wemhoner A., Ortner D., Tschirch E., Strasak A., Rudiger M. Nutrition of preterm infants in relation to bronchopulmonary dysplasia. BMC Pulm Med 2011, 11:7.
85. 2 exposure. Pediatr Res 1987, 21(2):109-115.
86. Delemos R.A., Coalson J.J., Gerstmann D.R., Kuehl T.J., Null D.M. Oxygen toxicity in the premature baboon with hyaline membrane disease. Am Rev Respir Dis 1987, 136(3):677-682.
87. Coalson J.J., Winter V., deLemos R.A. Decreased alveolarization in baboon survivors with bronchopulmonary dysplasia. Am J Respir Crit Care Med 1995, 152(2):640-646.
88. Warner B.B., Stuart L.A., Papes R.A., Wispe J.R. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol 1998, 275(1 Pt 1):L110-L117.
89. Coalson J.J. Experimental models of bronchopulmonary dysplasia. Biol Neonate 1997, 71(suppl. 1):35-38.
90. Buczynski B.W., Yee M., Paige Lawrence B., O'Reilly M.A. Lung development and the host response to influenza A virus are altered by different doses of neonatal oxygen in mice. Am J Physiol Lung Cell Mol Physiol 2012, 302(10):L1078-L1087.
91. O'Reilly M.A., Marr S.H., Yee M., McGrath-Morrow S.A., Lawrence B.P. Neonatal hyperoxia enhances the inflammatory response in adult mice infected with influenza A virus. Am J Respir Crit Care Med 2008, 177(10):1103-1110.
92. O'Reilly M.A., Yee M., Buczynski B.W., et al. Neonatal oxygen increases sensitivity to influenza A virus infection in adult mice by suppressing epithelial expression of Ear1. Am J Pathol 2012, 181(2):441-451.
93. Yee M., Chess P.R., McGrath-Morrow S.A., et al. Neonatal oxygen adversely affects lung function in adult mice without altering surfactant composition or activity. Am J Physiol Lung Cell Mol Physiol 2009, 297(4):L641-L649.
94. Yee M., White R.J., Awad H.A., Bates W.A., McGrath-Morrow S.A., O'Reilly M.A. Neonatal hyperoxia causes pulmonary vascular disease and shortens life span in aging mice. Am J Pathol 2011, 178(6):2601-2610.
95. Coalson J.J. Pathology of bronchopulmonary dysplasia. Semin Perinatol 2006, 30(4):179-184.
96. Rogers L.K., Tipple T.E., Nelin L.D., Welty S.E. Differential responses in the lungs of newborn mouse pups exposed to 85% or >95% oxygen. Pediatr Res. 2009, 65(1):33-38.
97. Breeze R.G., Wheeldon E.B. The cells of the pulmonary airways. Am Rev Respir Dis 1977, 116(4):705-777.
98. Kajekar R. Environmental factors and developmental outcomes in the lung. Pharmacol Ther 2007, 114(2):129-145.
99. Kleeberger S.R., Peden D. Gene-environment interactions in asthma and other respiratory diseases. Annu Rev Med 2005, 56:383-400.
100. Kabesch M. Gene by environment interactions and the development of asthma and allergy. Toxicol Lett 2006, 162(1):43-48.
101. Kho A.T., Bhattacharya S., Mecham B.H., Hong J., Kohane I.S., Mariani T.J. Expression profiles of the mouse lung identify a molecular signature of time-to-birth. Am J Respir Cell Mol Biol 2009, 40(1):47-57.
102. Maeda Y., Dave V., Whitsett J.A. Transcriptional control of lung morphogenesis. Physiol Rev 2007, 87(1):219-244.
103. Minoo P., Hamdan H., Bu D., Warburton D., Stepanik P., deLemos R. TTF-1 regulates lung epithelial morphogenesis. Dev Biol 1995, 172(2):694-698.
104. Whitsett J.A. Review: the intersection of surfactant homeostasis and innate host defense of the lung: lessons from newborn infants. Innate Immun 2010, 16(3):138-142.
105. Wert S.E., Dey C.R., Blair P.A., Kimura S., Whitsett J.A. Increased expression of thyroid transcription factor-1 (TTF-1) in respiratory epithelial cells inhibits alveolarization and causes pulmonary inflammation. Dev Biol 2002, 242(2):75-87.
106. DeFelice M., Silberschmidt D., DiLauro R., et al. TTF-1 phosphorylation is required for peripheral lung morphogenesis, perinatal survival, and tissue-specific gene expression. J Biol Chem 2003, 278(37):35574-35583.
107. Wan H., Kaestner K.H., Ang S.L., et al. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development 2004, 131(4):953-964.
108. Morrisey E.E., Hogan B.L. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 2010, 18(1):8-23.
109. Cho H.Y., Reddy S.P., Kleeberger S.R. Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal 2006, 8(1-2):76-87.
110. Cho H.Y., Reddy S.P., Debiase A., Yamamoto M., Kleeberger S.R. Gene expression profiling of NRF2-mediated protection against oxidative injury. Free Radic Biol Med 2005, 38(3):325-343.
111. Cho H.Y., Jedlicka A.E., Reddy S.P., et al. Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 2002, 26(2):175-182.
112. Marzec J.M., Christie J.D., Reddy S.P., et al. Functional polymorphisms in the transcription factor NRF2 in humans increase the risk of acute lung injury. FASEB J 2007, 21(9):2237-2246.
113. Hoffmann A., Baltimore D. Circuitry of nuclear factor kappaB signaling. Immunol Rev 2006, 210:171-186.
114. Dieperink H.I., Blackwell T.S., Prince L.S. Hyperoxia and apoptosis in developing mouse lung mesenchyme. Pediatr Res 2006, 59(2):185-190.
115. Bourbia A., Cruz M.A., Rozycki H.J. NF-kappaB in tracheal lavage fluid from intubated premature infants: association with inflammation, oxygen, and outcome. Arch Dis Child Fetal Neonatal Ed 2006, 91(1):F36-F39.
116. Cao L., Liu C., Cai B., et al. Nuclear factor-kappa B expression in alveolar macrophages of mechanically ventilated neonates with respiratory distress syndrome. Biol Neonate 2004, 86(2):116-123.
117. Ben-Ari J., Makhoul I.R., Dorio R.J., Buckley S., Warburton D., Walker S.M. Cytokine response during hyperoxia: sequential production of pulmonary tumor necrosis factor and interleukin-6 in neonatal rats. Isr Med Assoc J 2000, 2(5):365-369.
118. Yang G., Abate A., George A.G., Weng Y.H., Dennery P.A. Maturational differences in lung NF-kappaB activation and their role in tolerance to hyperoxia. J Clin Invest 2004, 114(5):669-678.
119. Das K.C., Ravi D., Holland W. Increased apoptosis and expression of p21 and p53 in premature infant baboon model of bronchopulmonary dysplasia. Antioxid Redox Signal 2004, 6(1):109-116.
120. Staversky R.J., Vitiello P.F., Yee M., Callahan L.M., Dean D.A., O'Reilly M.A. Epithelial ablation of Bcl-XL increases sensitivity to oxygen without disrupting lung development. Am J Respir Cell Mol Biol 2010, 43(3):376-385.
121. Vousden K.H., Prives C. Blinded by the light: the growing complexity of p53. Cell 2009, 137(3):413-431.
122. Matoba S., Kang J.G., Patino W.D., et al. p53 regulates mitochondrial respiration. Science 2006, 312(5780):1650-1653.
123. Ratner V., Starkov A., Matsiukevich D., Polin R.A., Ten V.S. Mitochondrial dysfunction contributes to alveolar developmental arrest in hyperoxia-exposed mice. Am J Respir Cell Mol Biol 2009, 40(5):511-518.
124. Alescio T., Cassini A. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. J Exp Zool 1962, 150:83-94.
125. Wessells N.K. Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool 1970, 175(4):455-466.
126. Adamson I.Y., Bowden D.H., Wyatt J.P. Oxygen poisoning in mice. Ultrastructural and surfactant studies during exposure and recovery. Arch Pathol 1970, 90(5):463-472.
127. Bowden D.H., Adamson I.Y., Wyatt J.P. Reaction of the lung cells to a high concentration of oxygen. Arch Pathol 1968, 86(6):671-675.
128. Adamson I.Y., Bowden D.H. The type 2 cell as progenitor of alveolar epithelial regeneration. A cytodynamic study in mice after exposure to oxygen. Lab Invest 1974, 30(1):35-42.
129. Roper J.M., Mazzatti D.J., Watkins R.H., Maniscalco W.M., Keng P.C., O'Reilly M.A. In vivo exposure to hyperoxia induces DNA damage in a population of alveolar type II epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004, 286(5):L1045-L1054.
130. Yam J., Frank L., Roberts R.J. Oxygen toxicity: comparison of lung biochemical responses in neonatal and adult rats. Pediatr Res 1978, 12(2):115-119.