Inhaled nitric oxide improves lung structure and pulmonary hypertension in a model of bleomycin-induced bronchopulmonary dysplasia in neonatal rats

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 6, 2009, Pages

  Tourneux, Pierre ^a,b   Markham, Neil ^a   Seedorf, Gregory ^a   Balasubramaniam, Vivek ^a   Abman, Steven H ^a  

^a Children's Hospital Colorado   (United States)

^b AMIENS UNIVERSITY HOSPITAL   (France)

Author keywords

Alveolarization; Lung development; Nitric oxide

Indexed keywords

BLEOMYCIN; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL WALL THICKNESS; ARTICLE; CONTROLLED STUDY; HEART RIGHT VENTRICLE HYPERTROPHY; LUNG BLOOD VESSEL; LUNG DYSPLASIA; LUNG STRUCTURE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; SPRAGUE DAWLEY RAT; TREATMENT DURATION;

ADMINISTRATION, INHALATION; ANIMALS; ANIMALS, NEWBORN; BLEOMYCIN; BODY WEIGHT; CELL COUNT; DISEASE MODELS, ANIMAL; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; LUNG; LUNG INJURY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; ORGAN SIZE; PULMONARY ALVEOLI; RATS; RATS, SPRAGUE-DAWLEY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 71949130151     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00293.2009     Document Type: Article

References (63)

1. Abe K, Shimokawa H, Morikawa K, Uwatoku T, Oi K, Matsumoto Y, Hattori T, Nakashima Y, Kaibuchi K, Sueishi K, Takeshit A. Longterm treatment with a Rho-kinase inhibitor improves monocrotaline-induced fatal pulmonary hypertension in rats. Circ Res 94: 385-393, 2004. (Pubitemid 38240731)
2. Abe K, Tawara S, Oi K, Hizume T, Uwatoku T, Fukumoto Y, Kaibuchi K, Shimokawa H. Long-term inhibition of Rho-kinase ameliorates hypoxia-induced pulmonary hypertension in mice. J Cardiovasc Pharmacol 48: 280-285, 2006. (Pubitemid 46066832)
3. Auten RL, Mason SN, Whorton MH, Lampe WR, Foster WM, Goldberg RN, Li B, Stamler JS, Auten KM. Inhaled ethyl nitrite prevents hyperoxia-impaired postnatal alveolar development in newborn rats. Am J Respir Crit Care Med 176: 291-299, 2007. (Pubitemid 47195880)
4. Balasubramaniam V, Maxey A, Abman S. Inhaled nitric oxide reverses hypoxia induced lung hypoplasia in endothelial nitric oxide synthase-deficient mice. Chest 128: 613S-614S, 2005. (Pubitemid 43054158)
5. Balasubramaniam V, Maxey AM, Morgan DB, Markham NE, Abman SH. Inhaled NO restores lung structure in eNOS-deficient mice recovering from neonatal hypoxia. Am J Physiol Lung Cell Mol Physiol 291: L119-L127, 2006.
6. Ballard RA, Truog WE, Cnaan A, Martin RJ, Ballard PL, Merrill JD, Walsh MC, Durand DJ, Mayock DE, Eichenwald EC, Null DR, Hudak ML, Puri AR, Golombek SG, Courtney SE, Stewart DL, Welty SE, Phibbs RH, Hibbs AM, Luan X, Wadlinger SR, Asselin JM, Coburn CE. Inhaled nitric oxide in preterm infants undergoing mechanical ventilation. N Engl J Med 355: 343-353, 2006. (Pubitemid 44127537)
7. Barrington KJ, Finer NN. Inhaled nitric oxide for respiratory failure in preterm infants. Cochrane Database Syst Rev 1: CD000509, doi: 10.1002/14651858.CD000509.pub3, 2007.
8. Bjorklund LJ, Ingimarsson J, Curstedt T, John J, Robertson B, Werner O, Vilstrup CT. Manual ventilation with a few large breaths at birth compromises the therapeutic effect of subsequent surfactant replacement in immature lambs. Pediatr Res 42: 348-355, 1997. (Pubitemid 27362732)
9. Bland RD, Albertine KH, Carlton DP, MacRitchie AJ. Inhaled nitric oxide effects on lung structure and function in chronically ventilated preterm lambs. Am J Respir Crit Care Med 172: 899-906, 2005.
10. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
11. Caulkett NA, Cribb PH, Haigh JC. Comparative cardiopulmonary effects of carfentanil-xylazine and medetomidine-ketamine used for immobilization of mule deer and mule deer/white-tailed deer hybrids. Can J Vet Res 64: 64-68, 2000.
12. Chaudhary NI, Schnapp A, Park JE. Pharmacologic differentiation of inflammation and fibrosis in the rat bleomycin model. Am J Respir Crit Care Med 173: 769-776, 2006.
13. Chen F, Gong L, Zhang L, Wang H, Qi X, Wu X, Xiao Y, Cai Y, Liu L, Li X, Ren J. Short courses of low-dose dexamethasone delay bleomycin-induced lung fibrosis in rats. Eur J Pharmacol 536: 287-295, 2006.
14. Chua F, Gauldie J, Laurent GJ. Pulmonary fibrosis: searching for model answers. Am J Respir Cell Mol Biol 33: 9-13, 2005. (Pubitemid 40961008)
15. Coalson JJ, Winter V, deLemos RA. Decreased alveolarization in baboon survivors with bronchopulmonary dysplasia. Am J Respir Crit Care Med 152: 640-646, 1995.
16. Cooney TP, Thurlbeck WM. The radial alveolar count method of Emery and Mithal: a reappraisal 1-postnatal lung growth. Thorax 37: 572-579, 1982.
17. Davis DW, Weidner DA, Holian A, McConkey DJ. Nitric oxide-dependent activation of p53 suppresses bleomycin-induced apoptosis in the lung. J Exp Med 192: 857-869, 2000. (Pubitemid 30737592)
18. Deruelle P, Grover TR, Abman SH. Pulmonary vascular effects of nitric oxide-cGMP augmentation in a model of chronic pulmonary hypertension in fetal and neonatal sheep. Am J Physiol Lung Cell Mol Physiol 289: L798-L806, 2005. (Pubitemid 41504411)
19. 2+ signaling in vascular endothelial cells. Am J Physiol Lung Cell Mol Physiol 270: L954-L961, 1996.
20. Gunther A, Lubke N, Ermert M, Schermuly RT, Weissmann N, Breithecker A, Markart P, Ruppert C, Quanz K, Ermert L, Grimminger F, Seeger W. Prevention of bleomycin-induced lung fibrosis by aerosolization of heparin or urokinase in rabbits. Am J Respir Crit Care Med 168: 1358-1365, 2003. (Pubitemid 37487332)
21. Hascoet JM, Fresson J, Claris O, Hamon I, Lombet J, Liska A, Cantagrel S, Al Hosri J, Thiriez G, Valdes V, Vittu G, Egreteau L, Henrot A, Buchweiller MC, Onody P. The safety and efficacy of nitric oxide therapy in premature infants. J Pediatr 146: 318-323, 2005. (Pubitemid 40341739)
22. Hemnes AR, Zaiman A, Champion HC. PDE5A inhibition attenuates bleomycin-induced pulmonary fibrosis and pulmonary hypertension through inhibition of ROS generation and RhoA/Rho kinase activation. Am J Physiol Lung Cell Mol Physiol 294: L24-L33, 2008.
23. Jernigan NL, O'Donaughy TL, Walker BR. Correlation of HO-1 expression with onset and reversal of hypoxia-induced vasoconstrictor hyporeactivity. Am J Physiol Heart Circ Physiol 281: H298-H307, 2001. (Pubitemid 32911804)
24. Kinsella JP, Cutter GR, Walsh WF, Gerstmann DR, Bose CL, Hart C, Sekar KC, Auten RL, Bhutani VK, Gerdes JS, George TN, Southgate WM, Carriedo H, Couser RJ, Mammel MC, Hall DC, Pappagallo M, Sardesai S, Strain JD, Baier M, Abman SH. Early inhaled nitric oxide therapy in premature newborns with respiratory failure. N Engl J Med 355: 354-364, 2006. (Pubitemid 44127538)
25. Kinsella JP, Greenough A, Abman SH. Bronchopulmonary dysplasia. Lancet 367: 1421-1431, 2006.
26. Kinsella JP, Parker TA, Galan H, Sheridan BC, Abman SH. Independent and combined effects of inhaled nitric oxide, liquid perfluorochemical, and high-frequency oscillatory ventilation in premature lambs with respiratory distress syndrome. Am J Respir Crit Care Med 159: 1220-1227, 1999. (Pubitemid 29202559)
27. Kinsella JP, Parker TA, Galan H, Sheridan BC, Halbower AC, Abman SH. Effects of inhaled nitric oxide on pulmonary edema and lung neutrophil accumulation in severe experimental hyaline membrane disease. Pediatr Res 41: 457-463, 1997. (Pubitemid 27147859)
28. Knepler JL Jr, Taher LN, Gupta MP, Patterson C, Pavalko F, Ober MD, Hart CM. Peroxynitrite causes endothelial cell monolayer barrier dysfunction. Am J Physiol Cell Physiol 281: C1064-C1075, 2001. (Pubitemid 32880912)
29. Kraybill EN, Runyan DK, Bose CL, Khan JH. Risk factors for chronic lung disease in infants with birth weights of 751 to 1000 grams. J Pediatr 115: 115-120, 1989.
30. Lin YJ, Markham NE, Balasubramaniam V, Tang JR, Maxey A, Kinsella JP, Abman SH. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr Res 58: 22-29, 2005. (Pubitemid 40967424)
31. MacRitchie AN, Albertine KH, Sun J, Lei PS, Jensen SC, Freestone AA, Clair PM, Dahl MJ, Godfrey EA, Carlton DP, Bland RD. Reduced endothelial nitric oxide synthase in lungs of chronically ventilated preterm lambs. Am J Physiol Lung Cell Mol Physiol 281: L1011-L1020, 2001. (Pubitemid 32948185)
32. Massaro GD, Olivier J, Massaro D. Brief perinatal hypoxia impairs postnatal development of the bronchiolar epithelium. Am J Physiol Lung Cell Mol Physiol 257: L80-L85, 1989. (Pubitemid 19234221)
33. McCurnin DC, Pierce RA, Chang LY, Gibson LL, Osborne-Lawrence S, Yoder BA, Kerecman JD, Albertine KH, Winter VT, Coalson JJ, Crapo JD, Grubb PH, Shaul PW. 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 288: L450-L459, 2005. (Pubitemid 40229510)
34. McNamara PJ, Murthy P, Kantores C, Teixeira L, Engelberts D, van Vliet T, Kavanagh BP, Jankov RP. Acute vasodilator effects of Rho-kinase inhibitors in neonatal rats with pulmonary hypertension unresponsive to nitric oxide. Am J Physiol Lung Cell Mol Physiol 294: L205-L213, 2008. (Pubitemid 351253358)
35. Meyrick B, Reid L. The effect of continued hypoxia on rat pulmonary arterial circulation. An ultrastructural study. Lab Invest 38: 188-200, 1978. (Pubitemid 8290111)
36. Molina-Molina M, Serrano-Mollar A, Bulbena O, Fernandez-Zabalegui L, Closa D, Marin-Arguedas A, Torrego A, Mullol J, Picado C, Xaubet A. Losartan attenuates bleomycin induced lung fibrosis by increasing prostaglandin E2 synthesis. Thorax 61: 604-610, 2006. (Pubitemid 44035141)
37. Moss TJ, Nitsos I, Kramer BW, Ikegami M, Newnham JP, Jobe AH. Intra-amniotic endotoxin induces lung maturation by direct effects on the developing respiratory tract in preterm sheep. Am J Obstet Gynecol 187: 1059-1065, 2002. (Pubitemid 35178411)
38. Murthy KS, Zhou H, Grider JR, Brautigan DL, Eto M, Makhlouf GM. Differential signaling by muscarinic receptors in smooth muscle: m2-mediated inactivation of myosin light chain kinase via Gi3, Cdc42/Rac1 and p21-activated kinase 1 pathway, and m3-mediated MLC20 (20-kDa regulatory light chain of myosin II) phosphorylation via Rho-associated kinase/myosin phosphatase targeting subunit 1 and protein kinase C/CPI-17 pathway. Biochem J 374: 145-155, 2003.
39. Neumann P, Gertzberg N, Johnson A. TNF-alpha induces a decrease in eNOS promoter activity. Am J Physiol Lung Cell Mol Physiol 286: L452-L459, 2004. (Pubitemid 38129528)
40. Northway WH Jr, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease. Bronchopulmonary dysplasia. N Engl J Med 276: 357-368, 1967.
41. Pinart M, Serrano-Mollar A, Negri EM, Cabrera R, Rocco PR, Romero PV. Inflammatory related changes in lung tissue mechanics after bleomycin-induced lung injury. Respir Physiol Neurobiol 160: 196-203, 2008. (Pubitemid 351173006)
42. Roberts JD Jr, Chiche JD, Weimann J, Steudel W, Zapol WM, Bloch KD. Nitric oxide inhalation decreases pulmonary artery remodeling in the injured lungs of rat pups. Circ Res 87: 140-145, 2000. (Pubitemid 30616910)
43. Roberts JD Jr, Roberts CT, Jones RC, Zapol WM, Bloch KD. Continuous nitric oxide inhalation reduces pulmonary arterial structural changes, right ventricular hypertrophy, and growth retardation in the hypoxic newborn rat. Circ Res 76: 215-222, 1995.
44. 2 response in newborn rats before and during anesthesia. J Appl Physiol 58: 1988-1996, 1985.
45. Sato S, Kato S, Arisaka Y, Takahashi H, Takahashi K, Tomoike H. Changes in pulmonary hemodynamics during normoxia and hypoxia in awake rats treated with intratracheal bleomycin. Tohoku J Exp Med 169: 233-244, 1993. (Pubitemid 23305713)
46. Scherle W. A simple method for volumetry of organs in quantitative stereology. Mikroskopie 26: 57-60, 1970.
47. 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 349: 2099-2107, 2003. (Pubitemid 37464534)
48. Shaul PW, North AJ, Brannon TS, Ujiie K, Wells LB, Nisen PA, Lowenstein CJ, Snyder SH, Star RA. Prolonged in vivo hypoxia enhances nitric oxide synthase type I and type III gene expression in adult rat lung. Am J Respir Cell Mol Biol 13: 167-174, 1995.
49. Singh IN, Sullivan PG, Hall ED. Peroxynitrite-mediated oxidative damage to brain mitochondria: Protective effects of peroxynitrite scavengers. J Neurosci Res 85: 2216-2223, 2007.
50. Tang JR, Le Cras TD, Morris KG Jr, Abman SH. Brief perinatal hypoxia increases severity of pulmonary hypertension after reexposure to hypoxia in infant rats. Am J Physiol Lung Cell Mol Physiol 278: L356-L364, 2000.
51. Tang JR, Markham NE, Lin YJ, McMurtry IF, Maxey A, Kinsella JP, Abman SH. 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 287: L344-L351, 2004. (Pubitemid 38943916)
52. Tang JR, Seedorf G, Balasubramaniam V, Maxey A, Markham N, Abman SH. Early inhaled nitric oxide treatment decreases apoptosis of endothelial cells in neonatal rat lungs after vascular endothelial growth factor inhibition. Am J Physiol Lung Cell Mol Physiol 293: L1271-L1280, 2007. (Pubitemid 350159411)
53. Thebaud B, Abman SH. Bronchopulmonary dysplasia: where have all the vessels gone? Roles of angiogenic growth factors in chronic lung disease. Am J Respir Crit Care Med 175: 978-985, 2007. (Pubitemid 46741748)
54. Thurlbeck WM. The internal surface area of nonemphysematous lungs. Am Rev Respir Dis 95: 765-773, 1967.
55. Ueda K, Cho K, Matsuda T, Okajima S, Uchida M, Kobayashi Y, Minakami H, Kobayashi K. A rat model for arrest of alveolarization induced by antenatal endotoxin administration. Pediatr Res 59: 396-400, 2006. (Pubitemid 43740077)
56. Upmacis RK, Deeb RS, Resnick MJ, Lindenbaum R, Gamss C, Mittar D, Hajjar DP. Involvement of the mitogen-activated protein kinase cascade in peroxynitrite-mediated arachidonic acid release in vascular smooth muscle cells. Am J Physiol Cell Physiol 286: C1271-C1280, 2004. (Pubitemid 38649977)
57. Van Meurs KP, Wright LL, Ehrenkranz RA, Lemons JA, Ball MB, Poole WK, Perritt R, Higgins RD, Oh W, Hudak ML, Laptook AR, Shankaran S, Finer NN, Carlo WA, Kennedy KA, Fridriksson JH, Steinhorn RH, Sokol GM, Konduri GG, Aschner JL, Stoll BJ, D'Angio CT, Stevenson DK. Inhaled nitric oxide for premature infants with severe respiratory failure. N Engl J Med 353: 13-22, 2005. (Pubitemid 41007803)
58. Vermeersch P, Buys E, Pokreisz P, Marsboom G, Ichinose F, Sips P, Pellens M, Gillijns H, Swinnen M, Graveline A, Collen D, Dewerchin M, Brouckaert P, Bloch KD, Janssens S. Soluble guanylate cyclase-alpha1 deficiency selectively inhibits the pulmonary vasodilator response to nitric oxide and increases the pulmonary vascular remodeling response to chronic hypoxia. Circulation 116: 936-943, 2007. (Pubitemid 47300918)
59. Watterberg KL, Demers LM, Scott SM, Murphy S. Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops. Pediatrics 97: 210-215, 1996. (Pubitemid 26049651)
60. Williams JH Jr, Bodell P, Hosseini S, Tran H, Baldwin KM. Haemodynamic sequelae of pulmonary fibrosis following intratracheal bleomycin in rats. Cardiovasc Res 26: 401-408, 1992.
61. Xu W, Liu L, Smith GC, Charles G. Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat Cell Biol 2: 339-345, 2000. (Pubitemid 30781090)
62. Yoshimura S, Nishimura Y, Nishiuma T, Yamashita T, Kobayashi K, Yokoyama M. Overexpression of nitric oxide synthase by the endothelium attenuates bleomycin-induced lung fibrosis and impairs MMP-9/TIMP-1 balance. Respirology 11: 546-556, 2006. (Pubitemid 44186259)
63. Young SL, Evans K, Eu JP. Nitric oxide modulates branching morphogenesis in fetal rat lung explants. Am J Physiol Lung Cell Mol Physiol 282: L379-L385, 2002. (Pubitemid 34654639)