Antenatal glucocorticoids counteract LPS changes in TGF-β pathway and caveolin-1 in ovine fetal lung

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 304, Issue 6, 2013, Pages

  Collins, Jennifer J P ^a   Kunzmann, Steffen ^b   Kuypers, Elke ^a   Kemp, Matthew W ^c   Speer, Christian P ^b   Newnham, John P ^c   Kallapur, Suhas G ^c,d   Jobe, Alan H ^c,d   Kramer, Boris W ^a,c  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Bronchopulmonary dysplasia; Chorioamnionitis; Intrauterine infection; Lipopolysaccharide; Lung development; Prematurity; Transforming growth factor

Indexed keywords

BETAMETHASONE; CAVEOLIN 1; CONNECTIVE TISSUE GROWTH FACTOR; DECAPENTAPLEGIC PROTEIN; GLUCOCORTICOID; LIPOPOLYSACCHARIDE; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ARTICLE; DOWNSTREAM PROCESSING; FEMALE; GESTATIONAL AGE; NONHUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SHEEP; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECT; FETOMATERNAL TRANSFUSION; FETUS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; LUNG; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PREGNANCY; PROTEIN PROCESSING;

ANIMALS; BETAMETHASONE; CAVEOLIN 1; CONNECTIVE TISSUE GROWTH FACTOR; FEMALE; FETUS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; INJECTIONS, INTRAMUSCULAR; LIPOPOLYSACCHARIDES; LUNG; MATERNAL-FETAL EXCHANGE; PHOSPHORYLATION; PREGNANCY; PROTEIN PROCESSING, POST-TRANSLATIONAL; SHEEP; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

MLCS; MLOWN;

EID: 84877147411     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00251.2012     Document Type: Article

References (51)

1. Alapati D, Rong M, Chen S, Hehre D, Rodriguez MM, Lipson KE, Wu S. Connective tissue growth factor antibody therapy attenuates hyperoxiainduced lung injury in neonatal rats. Am J Respir Cell Mol Biol 45: 1169-1177, 2011.
2. Barar J, Campbell L, Hollins AJ, Thomas NP, Smith MW, Morris CJ, Gumbleton M. Cell selective glucocorticoid induction of caveolin-1 and caveolae in differentiating pulmonary alveolar epithelial cell cultures. Biochem Biophys Res Commun 359: 360-366, 2007.
3. Bartram U, Speer CP. The role of transforming growth factor beta in lung development and disease. Chest 125: 754-765, 2003.
4. Been J, Degraeuwe P, Kramer B, Zimmermann L. Antenatal steroids and neonatal outcome after chorioamnionitis: a meta-analysis. Br J Gastroenterol 118: 113-122, 2011.
5. Beeton ML, Maxwell NC, Davies PL, Nuttall D, McGreal E, Chakraborty M, Spiller OB, Kotecha S. Role of pulmonary infection in the development of chronic lung disease of prematurity. Eur Respir J 37: 1424-1430, 2011.
6. Carlo WA, McDonald SA, Fanaroff AA, Vohr BR, Stoll BJ, Ehrenkranz RA, Andrews WW, Wallace D, Das A, Bell EF, Walsh MC, Laptook AR, Shankaran S, Poindexter BB, Hale EC, Newman NS, Davis AS, Schibler K, Kennedy KA, Sanchez PJ, Van Meurs KP, Goldberg RN, Watterberg KL, Faix RG, Frantz ID, 3rd, Higgins RD. Association of antenatal corticosteroids with mortality and neurodevelopmental outcomes among infants born at 22 to 25 weeks' gestation. J Am Med Assoc 306: 2348-2358, 2011.
7. Chen F, Desai TJ, Qian J, Niederreither K, Lu J, Cardoso WV. Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 134: 2969-2979, 2007.
8. Chen S, Rong M, Platteau A, Hehre D, Smith H, Ruiz P, Whitsett J, Bancalari E, Wu S. CTGF disrupts alveolarization and induces pulmonary hypertension in neonatal mice: implication in the pathogenesis of severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 300: L330-L340, 2011.
9. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5: 410-421, 2003.
10. Gantert M, Been JV, Gavilanes AW, Garnier Y, Zimmermann LJ, Kramer BW. Chorioamnionitis: a multiorgan disease of the fetus? J Perinatol Suppl 30: S21-S30, 2010.
11. Gauldie J, Galt T, Bonniaud P, Robbins C, Kelly M, Warburton D. Transfer of the active form of transforming growth factor-beta 1 gene to newborn rat lung induces changes consistent with bronchopulmonary dysplasia. Am J Pathol 163: 2575-2584, 2003.
12. Gauldie J, Galt T, Bonniaud P, Robbins C, Kelly M, Warburton D. Transfer of the active form of transforming growth factor-beta 1 gene to newborn rat lung induces changes consistent with bronchopulmonary dysplasia. Am J Pathol 163: 2575-2584, 2003.
13. Goldenberg RL, Andrews WW, Faye-Petersen OM, Cliver SP, Goepfert AR, Hauth JC. The Alabama preterm birth study: corticosteroids and neonatal outcomes in 23-to 32-week newborns with various markers of intrauterine infection. Am J Obstet Gynecol 195: 1020-1024, 2006.
14. Gosens R, Mutawe M, Martin S, Basu S, Bos ST, Tran T, Halayko AJ. Caveolae and caveolins in the respiratory system. Curr Mol Med 8: 741-753, 2008.
15. Gosens R, Stelmack GL, Bos ST, Dueck G, Mutawe MM, Schaafsma D, Unruh H, Gerthoffer WT, Zaagsma J, Meurs H, Halayko AJ. Caveolin-1 is required for contractile phenotype expression by airway smooth muscle cells. J Cell Mol Med 15: 2430-2442, 2011.
16. Ikegami M, Jobe AH, Newnham J, Polk DH, Willet KE, Sly P. Repetitive prenatal glucocorticoids improve lung function and decrease growth in preterm lambs. Am J Respir Crit Care Med 156: 178-184, 1997.
17. Jin Y, Lee SJ, Minshall RD, Choi AM. Caveolin-1: a critical regulator of lung injury. Am J Physiol Lung Cell Mol Physiol 300: L151-L160, 2011.
18. Jobe AH. Glucocorticoids, inflammation and the perinatal lung. Semin Neonatol 6: 331-342, 2001.
19. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 163: 1723-1729, 2001.
20. Knox IC Jr, Hoerner JK. The role of infection in premature rupture of the membranes. Am J Obstet Gynecol 59: 190-194, 1950.
21. Kotecha S, Wangoo A, Silverman M, Shaw RJ. Increase in the concentration of transforming growth factor beta-1 in bronchoalveolar lavage fluid before development of chronic lung disease of prematurity. J Pediatr 128: 464-469, 1996.
22. Kunzmann S, Collins JJ, Yang Y, Uhlig S, Kallapur SG, Speer CP, Jobe AH, Kramer BW. Antenatal inflammation reduces expression of caveolin-1 and influences multiple signaling pathways in preterm fetal lungs. Am J Respir Cell Mol Biol 45: 969-976, 2011.
23. Kunzmann S, Speer CP, Jobe AH, Kramer BW. Antenatal inflammation induced TGF-β1 but suppressed CTGF in preterm lungs. Am J Physiol Lung Cell Mol Physiol 292: L223-L231, 2007.
24. Kuypers E, Collins JJ, Kramer BW, Ofman G, Nitsos I, Pillow JJ, Polglase GR, Kemp MW, Newnham JP, Gavilanes AW, Nowacki R, Ikegami M, Jobe AH, Kallapur SG. Intra-amniotic LPS and antenatal betamethasone: inflammation and maturation in preterm lamb lungs. Am J Physiol Lung Cell Mol Physiol 302: L380-L389, 2012.
25. Leask A, Abraham DJ. All in the CCN family: essential matricellular signaling modulators emerge from the bunker. J Cell Sci 119: 4803-4810, 2006.
26. Lecart C, Cayabyab R, Buckley S, Morrison J, Kwong KY, Warburton D, Ramanathan R, Jones CA, Minoo P. Bioactive transforming growth factor-beta in the lungs of extremely low birthweight neonates predicts the need for home oxygen supplementation. Biol Neonate 77: 217-223, 2000.
27. Lee AJ, Lambermont VA, Pillow JJ, Polglase GR, Nitsos I, Newnham JP, Beilharz MW, Kallapur SG, Jobe AH, Kramer BW. Fetal responses to lipopolysaccharide-induced chorioamnionitis alter immune and airway responses in 7-week-old sheep. Am J Obstet Gynecol 204: 364 e317-e324, 2011.
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 25: 402-408, 2001.
29. Lv XJ, Li YY, Zhang YJ, Mao M, Qian GS. Over-expression of caveolin-1 aggravate LPS-induced inflammatory response in AT-1 cells via up-regulation of cPLA2/p38 MAPK. Inflamm Res 59: 531-541, 2010.
30. Massague J. TGF-beta signal transduction. Annu Rev Biochem 67: 753-791, 1998.
31. Massaro GD, Massaro D. Formation of alveoli in rats: postnatal effect of prenatal dexamethasone. Am J Physiol Lung Cell Mol Physiol 263: L37-L41, 1992.
32. McDevitt TM, Gonzales LW, Savani RC, Ballard PL. Role of endogenous TGF-β in glucocorticoid-induced lung type II cell differentiation. Am J Physiol Lung Cell Mol Physiol 292: L249-L257, 2007.
33. Murphy SH, Suzuki K, Downes M, Welch GL, De Jesus P, Miraglia LJ, Orth AP, Chanda SK, Evans RM, Verma IM. Tumor suppressor protein (p)53, is a regulator of NF-kappaB repression by the glucocorticoid receptor. Proc Natl Acad Sci USA 108: 17117-17122, 2011.
34. Nishioka M, Ogawa E, Kinose D, Haruna A, Ohara T, Ito I, Hoshino Y, Ito Y, Matsumoto H, Niimi A, Mio T, Chin K, Hirai T, Muro S, Mishima M. Lipopolysaccharide induced connective tissue growth factor gene expression in human bronchial epithelial cells. Respirology 15: 669-676, 2010.
35. Ogias D, Bitencourt B, Alvares EP, Gama P. Corticosteroids induce the differential expression of TGFbeta isoforms, receptors and signaling in the gastric mucosa of suckling rats. Regul Pept 135: 17-22, 2006.
36. Rao NA, McCalman MT, Moulos P, Francoijs KJ, Chatziioannou A, Kolisis FN, Alexis MN, Mitsiou DJ, Stunnenberg HG. Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res 21: 1404-1416, 2011.
37. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP. Caveolin-1 regulates transforming growth factor (TGF)-beta/ SMAD signaling through an interaction with the TGF-beta type I receptor. J Biol Chem 276: 6727-6738, 2001.
38. Ronnestad A, Abrahamsen TG, Medbo S, Reigstad H, Lossius K, Kaaresen PI, Engelund IE, Irgens LM, Markestad T. Septicemia in the first week of life in a Norwegian national cohort of extremely premature infants. Pediatrics 115: e262-e268, 2005.
39. Serra R, Pelton RW, Moses HL. TGF beta 1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures. Development 120: 2153-2161, 1994.
40. Smoak KA, Cidlowski JA. Mechanisms of glucocorticoid receptor signaling during inflammation. Mech Ageing Dev 125: 697-706, 2004.
41. Stoll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, Ehrenkranz RA, Lemons JA, Donovan EF, Stark AR, Tyson JE, Oh W, Bauer CR, Korones SB, Shankaran S, Laptook AR, Stevenson DK, Papile LA, Poole WK. Late-onset sepsis in very low birth weight neonates: the experience of the NICHD Neonatal Research Network. Pediatrics 110: 285-291, 2002.
42. Sweet DG, Huggett MT, Warner JA, Moss TJ, Kloosterboer N, Halliday HL, Newnham JP, Kallapur SG, Jobe AH, Kramer BW. Maternal betamethasone and chorioamnionitis induce different collagenases during lung maturation in fetal sheep. Neonatology 94: 79-86, 2008.
43. Syrkina O, Jafari B, Hales CA, Quinn DA. Oxidant stress mediates inflammation and apoptosis in ventilator-induced lung injury. Respirology 13: 333-340, 2008.
44. Van Marter LJ, Dammann O, Allred EN, Leviton A, Pagano M, Moore M, Martin C. Chorioamnionitis, mechanical ventilation, and postnatal sepsis as modulators of chronic lung disease in preterm infants. J Pediatr 140: 171-176, 2002.
45. Vicencio AG, Lee CG, Cho SJ, Eickelberg O, Chuu Y, Haddad GG, Elias JA. Conditional overexpression of bioactive transforming growth factor-beta1 in neonatal mouse lung: a new model for bronchopulmonary dysplasia? Am J Respir Cell Mol Biol 31: 650-656, 2004.
46. Viscardi RM. Perinatal inflammation and lung injury. Semin Fetal Neonat Med 17: 30-35, 2012.
47. Viscardi RM, Atamas SP, Luzina IG, Hasday JD, He JR, Sime PJ, Coalson JJ, Yoder BA. Antenatal Ureaplasma urealyticum respiratory tract infection stimulates proinflammatory, profibrotic responses in the preterm baboon lung. Pediatr Res 60: 141-146, 2006.
48. 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.
49. Wen FQ, Kohyama T, Skold CM, Zhu YK, Liu X, Romberger DJ, Stoner J, Rennard SI. Glucocorticoids modulate TGF-beta production. Inflammation 26: 279-290, 2002.
50. Willet KE, Jobe AH, Ikegami M, Kovar J, Sly PD. Lung morphometry after repetitive antenatal glucocorticoid treatment in preterm sheep. Am J Respir Crit Care Med 163: 1437-1443, 2001.
51. Williams TM, Lisanti MP. The Caveolin genes: from cell biology to medicine. Ann Med 36: 584-595, 2004.