Bronchopulmonary dysplasia and early prophylactic inhaled nitric oxide in preterm infants: Current concepts and future research strategies in animal models

Journal of Perinatal Medicine

Volumn 36, Issue 5, 2008, Pages 442-447

  Rieger Fackeldey, Esther ^a   Hentschel, Roland ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

3 nitrotyrosine; Alveolarization; Angiogenesis; Hyperoxia; Lung development; Nitric oxide synthase; Prematurity; Superoxide dismutase

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SUPEROXIDE DISMUTASE; VASCULOTROPIN;

CYTOTOXICITY; DRUG EFFICACY; GENE THERAPY; HUMAN; LUNG DYSPLASIA; LUNG LAVAGE; NONHUMAN; OXYGEN THERAPY; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ADMINISTRATION, INHALATION; ANIMALS; BRONCHODILATOR AGENTS; BRONCHOPULMONARY DYSPLASIA; HUMANS; HYPEROXIA; INFANT, NEWBORN; INFANT, PREMATURE; MODELS, ANIMAL; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGEN; SUPEROXIDE DISMUTASE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 51549087400     PISSN: 03005577     EISSN: 16193997     Source Type: Journal    
DOI: 10.1515/JPM.2008.065     Document Type: Review

References (50)

1. Afshar S, Gibson LL, Yuhanna IS, Sherman TS, Kerecman JD, Grubb PH, et al. Pulmonary NO synthase expression is attenuated in a fetal baboon model of chronic lung disease. Am J Physiol Lung Cell Mol Physiol. 2003;284:L749-58.
2. Auten RL, Mason SN, Whorton MH, Lampe WR, Foster WM, Goldberg RN, et al. Inhaled ethyl nitrite prevents hyperoxia-impaired postnatal alveolar development in newborn rats. Am J Respir Crit Care Med. 2007;176:291-9.
3. Ballard PL, Gonzales LW, Godinez RI, Godinez MH, Savani RC, McCurnin DC, et al. Surfactant composition and function in a primate model of infant chronic lung disease: effects of inhaled nitric oxide. Pediatr Res. 2006;59:157-62.
4. Ballard RA, Truog WE, Cnaan A, Martin RJ, Ballard PL, Merrill JD, et al., NO CLD Study Group. Inhaled nitric oxide in preterm infants undergoing mechanical ventilation. N Engl J Med. 2006;355:343-53.
5. Banks BA, Ischiropoulos H, McClelland M, Ballard PL, Ballard RA. Plasma 3-nitrotyrosine is elevated in premature infants who develop bronchopulmonary dysplasia. Pediatrics. 1998;101:870-4.
6. Bhandari V. The role of nitric oxide in hyperoxia-induced injury to the developing lung. Frontiers in Bioscience. 2003;8:361-9.
7. Bhatt AJ, Pryhuber GS, Huyck H, Watkins RH, Metlay LA, Maniscalco WM. 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. 2001;164:1971-80.
8. Bennet AJ, Shaw NJ, Gregg JE, Subhedar NV. Neurodevelopmental outcome in high-risk preterm infants treated with inhaled nitric oxide. Acta Paediatr. 2001;90:573-6.
9. Black SM, Heidersbach RS, McMullan DM, Becker JM, Johengen MJ, Fineman JR. Inhaled nitric oxide inhibits NOS activity in lambs: potential mechanism for rebound pulmonary hypertension. Am J Physiol. 1999;277:H1849-56.
10. Bonikos DS, Bensch KG, Ludwin SK, Northway WH. Oxygen toxicity in the newborn: the effect of prolonged 100 per cent O2 exposure on the lungs of newborn mice. Lab Invest. 1975;32:619-35.
11. Bucher JR, Roberts RJ. The development of the newborn rat lung in hyperoxia: a dose-response study of lung growth, maturation, and changes in antioxidant enzyme activities. Pediatr Res. 1981;15:999-1008.
12. Chang L, Ma L, Zhang X, Chen Y. The role of nitric oxide in hyperoxic lung injury in premature rats. J Tongji Med Univ. 2001;21:78-81.
13. Cheung PY, Peliowski A, Robertson CM. The outcome of very low birth weight neonates (≤1500 g) rescued by inhaled nitric oxide: neurodevelopment in early childhood. J Pediatr. 1998;133:735-9.
14. Couroucli XI, Wei YH, Jiang W, Muthiah K, Evey LW, Barrios R, et al. Modulation of pulmonary cytochrome P4501A1expression by hyperoxia and inhaled nitric oxide in the newborn rat: implications for lung injury. Pediatr Res. 2006;59:401-6.
15. Dauger S, Ferkdadji LF, Saumon G, Vardon G, Peuchmaur M, Gaultier C, et al. Neonatal exposure to 65% oxygen durably impairs lung architecture and breathing pattern in adult mice. Chest 2003;123:530-8.
16. Davis JM, Parad RB, Michele T, Allred E, Price E, Rosenfeld W, North American Recombinant Human CuZnSOD Study Group. Pulmonary outcome at one year corrected age in premature infants treated at birth with recombinant CuZn superoxide dismutase. Pediatrics. 2003;111:469-76.
17. Ekekezie II, Thibeault DW, Rezaiekhaligh MH, Mabry SM, Norberg M, Reddy GK, et al. High-dose inhaled nitric oxide and hyperoxia increases lung collagen accumulation in piglets. Biol Neonate. 2000;78:198-206.
18. Folz RJ, Abushamaa RM, Suliman HB. Extracellular superoxide dismutase in the airways of transgenic mice reduces inflammation and attenuates lung toxicity following hyperoxia. J Clin Invest. 1999;103:1055-66.
19. Fortenberry JD, Owens ML, Brown MR, Atkinson D, Brown LAS. Exogenous nitric oxide enhances neutrophil cell death and DNA fragmentation. Am J Respir Cell Mol Biol. 1998;18:421-8.
20. Franco-Belgium Collaborative NO Trial Group. Early compared with delayed inhaled nitric oxide in moderately hypoxaemic neonates with respiratory failure: a randomised controlled trial. Lancet. 1999;354:1066-71.
21. Franek WR, Chowdary YC, Lin X, Hu M, Miller EJ, Kazzaz JA, et al. Suppression of nuclear factor-kappa B activity by nitric oxide and hyperoxia in oxygen-resistant cells. J Biol Chem. 2002;277:4269-700.
22. Frank L, McLaughlin GE. Protection against acute and chronic hyperoxic inhibition of neonatal rat lung development with the 21-aminosteroid drug U74389F. Pediatr Res. 1993:33:632-8.
23. Hallman M, Waffarn F, Bry K, Turbow R, Kleinman MT, Mautz WJ, et al. Surfactant dysfunction after inhalation of nitric oxide. J Appl Physiol. 1996;80:2026-34.
24. Ter Horst SA, Walther FJ, Poorthuis BJ, Hiemstra PS, Wagenaar GT. Inhaled nitric oxide attenuates pulmonary inflammation and fibrin deposition and prolongs survival in neonatal hyperoxic lung injury. AJP-Lung Cell Mol Physiol. 2007;293:L35-44.
25. Hosford GE, Olson DM. Effects of hyperoxia on VEGF, ist receptors, and HIF-2alpha in the newborn rat lung. Am J Physiol Lung Cell Physiol. 2003;285:L161-8.
26. Howlett CE, Hutchison JS, Weinot JP, Chiu A, Merchant P, Fliss H. Inhaled nitric oxide protects against hyperoxia-induced apoptosis in rat lungs. Am J Physiol. 1999;277:L596-605.
27. Iben SC, Dreshaj IA, Farver CF, Haxhiu MA, Martin RJ. Role of endogenous nitric oxide in hyperoxia-induced airway hyperreactivity in maturing rats. J Appl Physiol. 2000;89:1205-12.
28. Issa A, Lappalainen U, Kleinman M, Bry K, Hallman M. Inhaled nitric oxide decreases hyperoxia-induced surfactant abnormality in preterm rabbits. Pediatr Res. 1999;45:247-54.
29. Jankov RP, Luo X, Campbell A, Belcastro R, Cabacungan J, Johnstone L, et al. Fibroblast growth factor receptor-1 and neonatal compensatory lung growth after exposure to 95% oxygen. Am J Respir Crit Care Med. 2003;167:1554-61.
30. Janssen-Heininger YM, Persinger RL, Korn SH, Pantano C, McElhinney B, Reynaert NL, et al. Reactive nitrogen species and cell signaling: implications for death or survival of lung epithelium. Am J Respir Crit Care Med. 2002;166:S9-16.
31. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2001;163:1723-9.
32. Kinsella JP, Cutter GR, Walsh WF, Gerstmann DR, Bose CL, Hart C, et al. Early inhaled nitric oxide therapy in premature newborns with respiratory failure. N Engl J Med. 2006;355:354-64.
33. Kunig AM, Balasubramaniam V, Markham NE, Morgan D, Montgomery G, Grover TR, et al. Recombinant human VEGF treatment enhances alveolarization after hyperoxic lung injury in neonatal rats. Am J Physiol Lung Cell Mol Physiol. 2005;289:L529-35.
34. Lin YJ, Markham NE, Balasubramaniam V, Tang JR, Maxey A, Kinsella JP, et al. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr Res. 2005;58:22-9.
35. McCurnin DC, Pierce RA, Chang LY, Gibson LL, Osborne-Lawrence S, Yoder BA, 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:L450-9.
36. Mestan KK, Marks JD, Hecox K, Huo D, Schreiber MD. Neurodevelopmental outcomes of premature infants treated with inhaled nitric oxide. N Engl J Med. 2005;353:23-32.
37. van Meurs KP, Wright LL, Ehrenkranz RA, Lemons JA, Ball MB, Poole WK, et al. for the Preemie Inhaled Nitric Oxide Study. Inhaled nitric oxide for premature infants with severe respiratory failure. N Engl J Med. 2005;353:13-21.
38. Munson DA, Grubb PH, Kerecman JD, McCurnin DC, Yoder BA, Hazen SL, et al. Pulmonary and systemic nitric oxide metabolites in a baboon model of neonatal chronic lung disease. Am J Respir Cell Mol Biol. 2005;33:582-8.
39. Ng YS, Rohan R, Sunday ME, Demello DE, D'Amore PA. Differential expressions of VEGF isoforms in mouse during development and in the adult. Dev Dyn. 2001;220:112-21.
40. Northway WH Jr, Rosan RC, Porter DY. Pulmonary disease following respiratory therapy of hyaline membrane disease. Bronchopulmonary Dysplasia. N Engl J Med. 1967;267:357-68.
41. Ohbayashi C, Kanomata N, Hanioka K, Itoh H. Airway lesions and superoxide dismutase distribution in bronchopulmonary dysplasia. Kobe J Med Sci. 1997;43:191-211.
42. Oury TD, Schaefer LM, Fattman CL, Choi A, Weck KE, Watkins SC. Depletion of pulmonary EC-SOD after exposure to hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2002;283:L777-84.
43. Park MS, Rieger-Fackeldey E, Schanbacher BL, Cook AC, Bauer JA, Rogers LK, et al. Altered expressions of fibroblast growth factor receptors and alveolarization in neonatal mice exposed to 85% oxygen. Pediatr Res. 2007, Oct 12 [Epub ahead of print].
44. Schreiber MD, Gin-Mestan K, Marks JD, Huo D, Lee G, Srisuparp P. Inhaled nitric oxide in premature infants with the respiratory distress syndrome. N Engl J Med. 2003;349:2099.
45. Shaul PW, Afshar S, Gibson LL, Sherman TS, Kerecman JD, Grubb PH, et al. Developmental changes in nitric oxide synthase isoform expression and nitric oxide production in fetal baboon lung. Am J Physiol Lung Cell Mol Physiol. 2002;283:L1192-9.
46. Sittipunt C, Steinberg KP, Ruzinsky JT, Myles C, Zhu S, Goodman RB, et al. Nitric oxide and nitrotyrosine in the lungs of patients with acute respiratory distress syndrome. Am J Respir Crit Care Med. 2001;163:503-10.
47. Stenmark KR, Abman SH. Lung vascular development: implications for the pathogenesis of bronchopulmonary dysplasia. Annu Rev Physiol. 2005;67:623-61.
48. Tang JR, Markham NE, Lin YJ, McMurtry IF, Maxey A, Kinsella JP, et al. Inhaled nitric oxide attenuates pulmonary hypertension and improves lung growth in infant rats after neonatal treatment with a VEGF receptor inhibitor. Am J Physiol Lung Cell Mol Physiol. 2004;287:L344-51.
49. Thébaud B, Ladha F, Michelakis ED, Sawicka M, Thurston G, Eaton F, et al. Vascular endothelial growth factor gene therapy increases survival, promotes lung angiogenesis, and prevents alveolar damage in hyperoxia-induced lung injury. Circulation. 2005;112:2477-86.
50. Warner BB, Stuart LA, Papes RA, Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol. 1998;275:L110-7.