VARA attenuates hyperoxia-induced impaired alveolar development and lung function in newborn mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 304, Issue 11, 2013, Pages

  James, Masheika L ^a,c   Catharine Ross, A ^b   Nicola, Teodora ^c   Steele, Chad ^d   Ambalavanan, Namasivayam ^a,c,e  

^a University of Alabama at Birmingham   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

10:1 molar combination of Vitamin A and all trans retinoic acid; 8 OH deoxyguanosine; Bronchopulmonary dysplasia; Nuclear factor (erythroid derived 2) like 2 protein; Retinoic acid; Vitamin A

Indexed keywords

3 NITROTYROSINE; CARBONYL DERIVATIVE; CXCL2 CHEMOKINE; CYTOKINE; EOTAXIN; GAMMA INTERFERON; MALONALDEHYDE; MESSENGER RNA; MYELOPEROXIDASE; RETINOIC ACID; RETINOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DNA DAMAGE; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPEROXIA; LUNG ALVEOLUS; LUNG COMPLIANCE; LUNG DEVELOPMENT; LUNG DYSPLASIA; LUNG FUNCTION; LUNG HOMOGENATE; LUNG RESISTANCE; MOUSE; NEWBORN; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

10:1 MOLAR COMBINATION OF VITAMIN A AND ALL-TRANS RETINOIC ACID; 8-OH DEOXYGUANOSINE; BRONCHOPULMONARY DYSPLASIA; NUCLEAR FACTOR (ERYTHROID-DERIVED 2)-LIKE 2 PROTEIN; RETINOIC ACID; VITAMIN A;

ANIMALS; ANIMALS, NEWBORN; FEMALE; HYPEROXIA; INFLAMMATION MEDIATORS; LUNG; LUNG COMPLIANCE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PLATELET-DERIVED GROWTH FACTOR; PULMONARY ALVEOLI; RNA, MESSENGER; TENASCIN; TRETINOIN; VITAMIN A; VITAMIN A DEFICIENCY;

EID: 84878654636     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00257.2012     Document Type: Article

References (47)

1. Acin-Perez R, Hoyos B, Zhao F, Vinogradov V, Fischman DA, Harris RA, Leitges M, Wongsiriroj N, Blaner WS, Manfredi G, Hammerling U. Control of oxidative phosphorylation by vitamin A illuminates a fundamental role in mitochondrial energy homoeostasis. FASEB J 24: 627-636, 2010.
2. Ambalavanan N, Carlo WA. Bronchopulmonary dysplasia: new insights. Clin Perinatol 31: 613-628, 2004.
3. Ambalavanan N, Carlo WA, Bobashev G, Mathias E, Liu B, Poole K, Fanaroff AA, Stoll BJ, Ehrenkranz R, Wright LL. Prediction of death for extremely low birth weight neonates. Pediatrics 116: 1367-1373, 2005.
4. 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 123: 1132-1141, 2009.
5. Ambalavanan N, Nicola T, Hagood J, Bulger A, Serra R, Murphy-Ullrich J, Oparil S, Chen YF. Transforming growth factor-beta signaling mediates hypoxia-induced pulmonary arterial remodeling and inhibition of alveolar development in newborn mouse lung. Am J Physiol Lung Cell Mol Physiol 295: L86-L95, 2008.
6. Ambalavanan N, Tyson JE, Kennedy KA, Hansen NI, Vohr BR, Wright LL, Carlo WA, National Institute of Child Health and Human Development Neonatal Research N. Vitamin A supplementation for extremely low birth weight infants: outcome at 18 to 22 months. Pediatrics 115: e249-e254, 2005.
7. Auten RL, Whorton MH, Nicholas Mason S. Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol 26: 391-397, 2002.
8. Bancalari E, Claure N, Sosenko IR. Bronchopulmonary dysplasia: changes in pathogenesis, epidemiology and definition. Semin Neonatol 8: 63-71, 2003.
9. Barker GF, Manzo ND, Cotich KL, Shone RK, Waxman AB. DNA damage induced by hyperoxia: quantitation and correlation with lung injury. Am J Respir Cell Mol Biol 35: 277-288, 2006.
10. Boucherat O, Franco-Montoya ML, Thibault C, Incitti R, Chailley-Heu B, Delacourt C, Bourbon JR. Gene expression profiling in lung fibroblasts reveals new players in alveolarization. Physiol Genomics 32: 128-141, 2007.
11. Bourbon J, Boucherat O, Chailley-Heu B, Delacourt C. Control mechanisms of lung alveolar development and their disorders in bronchopulmonary dysplasia. Pediatr Res 57: 38R-46R, 2005.
12. Bry K, Lappalainen U. Pathogenesis of bronchopulmonary dysplasia: the role of interleukin 1beta in the regulation of inflammation-mediated pulmonary retinoic acid pathways in transgenic mice. Semin Perinatol 30: 121-128, 2006.
13. Burri PH. Structural aspects of prenatal and postnatal development and growth for the lung. In: Lung Growth and Development, edited by McDonald SA. New York, NY: Dekker, 1997, p. 1-35.
14. 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 295: L584-L592, 2008.
15. Coalson JJ. Pathology of new bronchopulmonary dysplasia. Semin Neonatol 8: 73-81, 2003.
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. Couroucli XI, Liang YW, Jiang W, Barrios R, Moorthy B. Attenuation of oxygen-induced abnormal lung maturation in rats by retinoic acid: possible role of cytochrome P4501A enzymes. J Pharmacol Exp Ther 317: 946-954, 2006.
18. Darlow BA, Graham PJ. Vitamin A supplementation to prevent mortality and short and long-term morbidity in very low birthweight infants. Cochrane Database Syst Rev CD000501, 2007.
19. Deng H, Mason SN, Auten RL Jr. Lung inflammation in hyperoxia can be prevented by antichemokine treatment in newborn rats. Am J Respir Crit Care Med 162: 2316-2323, 2000.
20. Dirami G, Massaro GD, Clerch LB, Ryan US, Reczek PR, Massaro D. Lung retinol storing cells synthesize and secrete retinoic acid, an inducer of alveolus formation. Am J Physiol Lung Cell Mol Physiol 286: L249-L256, 2004.
21. Fisher Oxygen therapy AB. Side effects and toxicity. Am Rev Respir Dis 122: 61-69, 1980.
22. Freeman BA, Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 256: 10986-10992, 1981.
23. Goh FG, Piccinini AM, Krausgruber T, Udalova IA, Midwood KS. Transcriptional regulation of the endogenous danger signal tenascin-C: a novel autocrine loop in inflammation. J Immunol 184: 2655-2662, 2010.
24. Halliwell B, Gutteridge JMC. Free Radicals In Biology And Medicine. New York, NY: Oxford, 2007.
25. Hogmalm A, Backstrom E, Bry M, Lappalainen U, Lukkarinen HP, Bry K. Role of CXC chemokine receptor-2 in a murine model of bronchopulmonary dysplasia. Am J Respir Cell Mol Biol 47: 746-758, 2012.
26. James ML, Ross AC, Bulger A, Philips JB, 3rd, Ambalavanan N. Vitamin A and retinoic acid act synergistically to increase lung retinyl esters during normoxia and reduce hyperoxic lung injury in newborn mice. Pediatr Res 67: 591-597, 2010.
27. Jobe AJ. The new BPD: an arrest of lung development. Pediatr Res 46: 641-643, 1999.
28. Joung KE, Kim HS, Lee J, Shim GH, Choi CW, Kim EK, Kim BI, Choi JH. Correlation of urinary inflammatory and oxidative stress markers in very low birth weight infants with subsequent development of bronchopulmonary dysplasia. Free Rad Res 45: 1024-1032, 2011.
29. Konsavage W, Zhang L, Vary T, Shenberger JS. Hyperoxia inhibits protein synthesis and increases eIF2alpha phosphorylation in the newborn rat lung. Am J Physiol Lung Cell Mol Physiol 298: L678-L686, 2010.
30. Kumarasamy A, Schmitt I, Nave AH, Reiss I, van der Horst I, Dony E, Roberts JD, de Krijger RR, Tibboel D, Seeger W, Schermuly RT, Eickelberg O, Morty RE. Lysyl oxidase activity is dysregulated during impaired alveolarization of mouse and human lungs. Am J Respir Crit Care Med 180: 1239-1252, 2009.
31. Maden M. Retinoids in lung development and regeneration. Curr Top Dev Biol 61: 153-189, 2004.
32. Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell 83: 841-850, 1995.
33. Massaro D, Massaro GD. Invited Review: pulmonary alveoli: formation, the "call for oxygen, " and other regulators. Am J Physiol Lung Cell Mol Physiol 282: L345-L358, 2002.
34. Massaro GD, Massaro D, Chan WY, Clerch LB, Ghyselinck N, Chambon P, Chandraratna RA. Retinoic acid receptor-beta: an endogenous inhibitor of the perinatal formation of pulmonary alveoli. Physiol Genomics 4: 51-57, 2000.
35. McGowan S, Jackson SK, Jenkins-Moore M, Dai HH, Chambon P, Snyder JM. Mice bearing deletions of retinoic acid receptors demonstrate reduced lung elastin and alveolar numbers. Am J Respir Cell Mol Biol 23: 162-167, 2000.
36. Nicola T, Ambalavanan N, Zhang W, James ML, Rehan V, Halloran B, Olave N, Bulger A, Oparil S, Chen YF. Hypoxia-induced inhibition of lung development is attenuated by the peroxisome proliferator-activated receptor-γ agonist rosiglitazone. Am J Physiol Lung Cell Mol Physiol 301: L125-L134, 2011.
37. Nicola T, Hagood JS, James ML, Macewen MW, Williams TA, Hewitt MM, Schwiebert L, Bulger A, Oparil S, Chen YF, Ambalavanan N. Loss of Thy-1 inhibits alveolar development in the newborn mouse lung. Am J Physiol Lung Cell Mol Physiol 296: L738-L750, 2009.
38. Pappas CT, Obara H, Bensch KG, Northway WH Jr. Effect of prolonged exposure to 80% oxygen on the lung of the newborn mouse. Lab Invest 48: 735-748, 1983.
39. Perl AK, Gale E. FGF signaling is required for myofibroblast differentiation during alveolar regeneration. Am J Physiol Lung Cell Mol Physiol 297: L299-L308, 2009.
40. Rosales FJ, Ritter SJ, Zolfaghari R, Smith JE, Ross AC. Effects of acute inflammation on plasma retinol, retinol-binding protein, and its mRNA in the liver and kidneys of vitamin A-sufficient rats. J Lipid Res 37: 962-971, 1996.
41. Ross AC, Ambalavanan N, Zolfaghari R, Li NQ. Vitamin A combined with retinoic acid increases retinol uptake and lung retinyl ester formation in a synergistic manner in neonatal rats. J Lipid Res 47: 1844-1851, 2006.
42. Shea LM, Beehler C, Schwartz M, Shenkar R, Tuder R, Abraham E. Hyperoxia activates NF-kappaB and increases TNF-alpha and IFN-gamma gene expression in mouse pulmonary lymphocytes. J Immunol 157: 3902-3908, 1996.
43. Shenai JP, Chytil F, Stahlman MT. Vitamin A status of neonates with bronchopulmonary dysplasia. Pediatr Res 19: 185-188, 1985.
44. Thurlbeck WM. Postnatal growth and development of the lung. Am Rev Respir Dis 111: 803-844, 1975.
45. Tyson JE, Wright LL, Oh W, Kennedy KA, Mele L, Ehrenkranz RA, Stoll BJ, Lemons JA, Stevenson DK, Bauer CR, Korones SB, Fanaroff AA. Vitamin A supplementation for extremely-low-birthweight infants. National Institute of Child Health and Human Development Neonatal Research Network. N Engl J Med 340: 1962-1968, 1999.
46. Veness-Meehan KA, Pierce RA, Moats-Staats BM, Stiles AD. Retinoic acid attenuates O2-induced inhibition of lung septation. Am J Physiol Lung Cell Mol Physiol 283: L971-L980, 2002.
47. Zhu YK, Liu X, Ertl RF, Kohyama T, Wen FQ, Wang H, Spurzem JR, Romberger DJ, Rennard SI. Retinoic acid attenuates cytokinedriven fibroblast degradation of extracellular matrix in three-dimensional culture. Am J Respir Cell Mol Biol 25: 620-627, 2001.