Inhibition of β-catenin signaling improves alveolarization and reduces pulmonary hypertension in experimental bronchopulmonary dysplasia

American Journal of Respiratory Cell and Molecular Biology

Volumn 51, Issue 1, 2014, Pages 104-113

  Alapati, Deepthi ^a   Rong, Min ^a   Chen, Shaoyi ^a   Hehre, Dorothy ^a   Hummler, Stefanie C ^a   Wu, Shu ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Bronchopulmonary dysplasia; Hyperoxia; Neonatal lung injury; Pulmonary hypertension; catenin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA CATENIN; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; ICG 001; PROTEIN INHIBITOR; RESPIRATORY TRACT AGENT; SURFACTANT PROTEIN C; UNCLASSIFIED DRUG;

AIRWAY REMODELING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYPEROXIA; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS CELL; LUNG BLOOD VESSEL; LUNG DYSPLASIA; NEWBORN; NONHUMAN; PHARMACOLOGICAL BLOCKING; PREMATURITY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION;

BRONCHOPULMONARY DYSPLASIA; HYPEROXIA; NEONATAL LUNG INJURY; PULMONARY HYPERTENSION; Β-CATENIN;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BETA CATENIN; BICYCLO COMPOUNDS, HETEROCYCLIC; BLOTTING, WESTERN; BRONCHOPULMONARY DYSPLASIA; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; HYPEROXIA; HYPERTENSION, PULMONARY; IMMUNOENZYME TECHNIQUES; MYOCYTES, SMOOTH MUSCLE; PULMONARY ALVEOLI; PYRIMIDINONES; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84903716522     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0346OC     Document Type: Article

References (57)

1. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;163:1723-1729. (Pubitemid 32578778)
2. Bhandari A, Bhandari V. Pitfalls, problems, and progress in bronchopulmonary dysplasia. Pediatrics 2009;123:1562-1573.
3. Van Marter LJ. Epidemiology of bronchopulmonary dysplasia. Semin Fetal Neonatal Med 2009;14:358-366.
4. Husain AN, Siddiqui NH, Stocker JT. Pathology of arrested acinar development in post surfactant bronchopulmonary dysplasia. Hum Pathol 1998;29:710-717. (Pubitemid 28322056)
5. Jobe A. The new BPD: an arrest of lung development. Pediatr Res 1999; 46:641-643.
6. Stenmark KR, Abman SH. Lung vascular development: implications for pathogenesis of bronchopulmonary dysplasia. Annu Rev Physiol 2005;67:623-661. (Pubitemid 40404504)
7. 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 2007;175:978-985. (Pubitemid 46741748)
8. Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actinfilament assembly. Cell 2005;123:903-915. (Pubitemid 41721035)
9. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. Deconstructing the cadherin-catenin-actin complex. Cell 2005;123:889-901. (Pubitemid 41721034)
10. Lilien J, Balsamo J. The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of β-catenin. Curr Opin Cell Biol 2005;17:459-465. (Pubitemid 41267159)
11. Nelson WJ, Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004;303:1483-1487. (Pubitemid 38314410)
12. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469-480.
13. Willert K, Jones KA. Wnt signaling: is the party in the nucleus? Genes Dev 2006;20:1394-1404. (Pubitemid 43830647)
14. Oloumi A, Syam S, Dedhar S. Modulation of Wnt3a-mediated nuclear β-catenin accumulation and activation by integrin-linked kinase in mammalian cells. Oncogene 2006;25:7747-7757. (Pubitemid 44967969)
15. Oloumi A, McPhee T, Dedhar S. Regulation of E-cadherin expression and β-catenin/Tcf transcriptional activity by the integrin-linked kinase. Biochim Biophys Acta 2004;1691:1-15.
16. Hecht A, Vleminckx K, Stemmler MP, van Roy F, Kemler R. The acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EBMO J 2000;19:1839-1850. (Pubitemid 30204395)
17. Takemaru KI, Moon RT. The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J Cell Biol 2000;149: 249-254. (Pubitemid 30227143)
18. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. WNT and β-catenin signaling: diseases and therapies. Nat Rev Genet 2004;5: 691-701. (Pubitemid 39150127)
19. Mucenski ML, Wert SE, Nation JM, Loudy DE, Huelsken J, Birchmeier W, Morrisey EE, Whitsett JA. Beta-catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J Biol Chem 2003;278:40231-40238. (Pubitemid 37248591)
20. Königshoff M, Eickelberg O. Wnt signaling in lung disease: a failure or a regeneration signal? Am J Respir Cell Mol Biol 2010;42: 21-31.
21. Chilose M, Poletti V, Zamo A, Lestani M, Montagna L, Piccoli P, Pedron S, Bertaso M, Scarpa A, Murer B, et al. Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am J Pathol 2003;162:1495-1502. (Pubitemid 36512831)
22. Douglas IS, del Valle FD, Winn RA, Voelkel NF. β-catenin in the fibroproliferative response to acute lung injury. Am J Respir Cell Mol Biol 2006;34:274-285.
23. Zhou B, Liu Y, Kahn M, Ann DK, Han A, Wang HA, Nguyen C, Flodby P, Zhong Q, Krishnaveni MS, et al. Interactions between β-catenin and transforming growth factor-β signaling pathways mediate epithelial-mesenchymal transition and are dependent on the transcriptional co-activator cAMP-response element-binding protein (CREB)-binding protein (CBP). J Biol Chem 2012;287:7026-7038.
24. Lam AP, Gottardi CJ. β-catenin signaling: a novel mediator of fibrosis and potential therapeutic target. Curr Opin Rheumatol 2011;23: 562-567.
25. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M, Moon RT, Teo JL, Kim HY, Moon SH, et al. A small molecular inhibitor of β-catenin/CREB- binding protein transcription. Proc Natl Acad Sci USA 2004;101:12682-12687. (Pubitemid 39122083)
26. Henderson WR, Chi EY, Ye X, Nguyen C, Tien YT, Zhou B, Borok Z, Knight DA, Kahn M. Inhibition of Wnt/β-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc Natl Acad Sci USA 2010;107:14309-14314.
27. Alapati D, Min R, Chen S, Hehre D, Rodriguez MM, Lipson KE, Wu S. Connective tissue growth factor antibody therapy attenuates hyperoxia-induced lung injury in neonatal rats. Am J Respir Cell Mol Biol 2011;45:1169-1177.
28. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday J, Rehan V. Hyperoxia-induced neonatal rat lung injury involves activation of TGF-β and Wnt signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2009;296: L1031-L1041.
29. Popova AP, Bentley JK, Anyanwu AC, Richardson MN, Linn MJ, Lei J, Wong EJ, Goldsmith AM, Pryhuber GS, Hershenson MB. Glycogen synthase kinase-3β/β-catenin signaling regulates neonatal lung mesenchymal stromal cell myofibroblastic differentiation. Am J Physiol Lung Cell Mol Physiol 2012;303:L439-L448.
30. Chen S, Rong M, Platteau A, Hehre D, Smith H, Ruiz P, Whitsett J, Bancalari E, Wu S. CTGF disrupts alveolarization and induces PH in neonatal mice: implication in the pathogenesis of severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2011;300:L330-L340.
31. Hummler SC, Rong M, Chen S, Hehre D, Alapati D, Wu S. Targeting GSK-3β to prevent hyperoxia-induced lung injury in neonatal rats. Am J Respir Cell Mol Biol 2013;48:578-588.
32. Tanaka A, Jin Y, Lee SJ, Zhang M, Kim HP, Stolz DB, Ryter SW, Choi AM. Hyperoxia-induced LC3B interacts with the Fas apoptotic pathway in epithelial cell death. Am J Respir Cell Mol Biol 2012;46:507-514.
33. Gradl D, Kuhl M, Wedlich D. The Wnt/Wg signal transducer β-catenin controls fibronectin expression. Mol Cell Biol 1999;19:5576-5587. (Pubitemid 29339915)
34. Chiang HY, Korshunov VA, Serour A, Shi F, Sottile J. Fibronectin is an important regulator of flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol 2009;29:1074-1079.
35. Huang BL, Brugger SM, Lyons KM. Stage-specific control of connective tissue growth factor (CTGF/CCN2) expression in chondrocytes by Sox9 and β-catenin. J Biol Chem 2010;285: 27702-27712.
36. Fan WH, Pech M, Karnovsky MJ. Connective tissue growth factor (CTGF) stimulates vascular smooth muscle cell growth and migration in vitro. Eur J Cell Biol 2000;79:915-923. (Pubitemid 32000725)
37. Eguchi M, Nguyen C, Lee SC, Kahn M. ICG-001, a novel small molecule regulator of TCF/beta-catenin transcription. Med Chem 2005;1:467-472.
38. Teo JL, Ma H, Nguyen C, Lam C, Kahn M. Specific inhibition of CBP/β-catenin interaction rescues defects in neuronal differentiation by a presenilin-1 mutation. Proc Natl Acad Sci USA 2005;102: 12171-12176. (Pubitemid 41291147)
39. Kim H, Won S, Hwang DY, Lee JS, Kim M, Kim R, Kim W, Cha B, Kim T, Costantini F, et al. Downregulation of Wnt/β-catenin signaling causes degeneration of hippocampal neurons in vivo. Neurobiol Aging 2011;32:2316.e1-e15.
40. Yan D, Avtanski D, Saxena NK, Sharma D. Leptin-induced epithelialmesenchymal transition in breast cancer cells requires β-catenin activation via Akt/GSK3-dependent and MTA/Wnt1-dependent pathways. J Biol Chem 2012;287:8598-8612.
41. Alapati D, Rong M, Chen S, Lin C, Li Y, Wu S. Inhibition of LRP5/6-mediated Wnt/β-catenin signaling by Mesd attenuates hyperoxia-induced pulmonary hypertension in neonatal rats. Pediatr Res 2013;73:719-725.
42. Khemani E, McElhinney DB, Rhein L, Andrade O, Lacro RV, Thomas KC, Mullen MP. Pulmonary artery hypertension in formerly premature infants with bronchopulmonary dysplasia: clinical features and outcomes in the surfactant era. Pediatrics 2007;120:1260-1269. (Pubitemid 350223677)
43. Haworth SG. Pulmonary vascular remodeling in neonatal pulmonary artery hypertension, state of art. Chest 1988;93:133S-138S.
44. del Cerro MJ, Rotes AS, Carton A, Deiros L, Bret M, Cordeiro M, Verdu C, Barrios MI, Albajara L, Gutierrez-Larraya F. Pulmonary hypertension in bronchopulmonary dysplasia: clinical findings, cardiovascular anomalies and outcomes. Pediatr Pulmonol 2014;49:49-59.
45. Mourani PM, Abman SH. Pulmonary vascular disease in bronchopulmonary dysplasia: pulmonary hypertension and beyond. Curr Opin Pediatr 2013;25:329-337.
46. Yee M, White RJ, Awad HA, Bates WA, Mcgrath-Morrow SA, O'Reilly MA. Neonatal hyperoxia causes pulmonary vascular disease and shortens life span in aging mice. Am J Pathol 2011;178:2601-2610.
47. Aslam M, Baveja R, Liang OD, Fernandez-Gonzalez A, Lee C, Mitsialis SA, Kourembanas S. None marrow stromal cells attenuate lung injury in a murine model neonatal chronic lung disease. Am J Respir Crit Care Med 2009;180:1122-1130.
48. Ghofrani HA, Seeger W, Grimminger F. Imatinib for the treatment of pulmonary arterial hypertension. N Engl J Med 2005;353: 1412-1413. (Pubitemid 41362714)
49. Frenckner B, Broome M, Lindstrom M, Radell P. Platelet-derived growth factor inhibition: a new treatment of pulmonary hypertension in congenital diaphragmatic hernia? J Pediatr Surg 2008;43: 1928-1931.
50. Uglow EB, Slater S, Sala-Newby GB, Aguilera-Garcia CM, Angelini GD, Newby AC, George SJ. Dismantling of cadherin-mediated cell-cell contacts modulates smooth muscle proliferation. Circ Res 2003;92: 1314-1321. (Pubitemid 36773473)
51. Slater SC, Koutsouki E, Jackson CL, Bush RC, Angelini GD, Newby AC, George SJ. R-cadherin: β-catenin complex and its association with vascular smooth muscle cell proliferation. Arterioscler Thromb Vasc Biol 2004;24:1204-1210. (Pubitemid 38880009)
52. Blidt R, Bosserhoff A-K, Dammers J, Krott N, Demircan L, Hoffmann R, Hanrath P, Weber C, Vogt F. Downregulation of N-cadherin in the neointima stimulates migration of smooth muscle cells by RhoA deactivation. Cardiovasc Res 2004;62:212-222. (Pubitemid 38326827)
53. Jones M, Sabatini PJ, Lee FS, Bendeck MP, Langille BL. N-cadherin upregulation and function in response of smooth muscle cells to arterial injury. Arterioscler Thromb Vasc Biol 2002;22:1972-1977. (Pubitemid 36025201)
54. Quasnichka H, Slater SC, Beeching CA, Boehm M, Sala-Newby GB, George S. Regulation of smooth muscle cell proliferation by β-catenin/TCF signaling involves modulation of cyclin D1 and p21 expression. Circ Res 2006;99:1329-1337. (Pubitemid 44949668)
55. Wang X, Xiao Y, Mou Y, Zhao Y, Blankesteijn M, Hall JL. A role for the β-catenin/TCF signaling cascade in vascular remodeling. Circ Res 2002;90:340-347. (Pubitemid 34633936)
56. Hussain N, Wu F, Christian C, Kresch MJ. Hyperoxia inhibits fetal rat lung fibroblast proliferation and expression of procollagens. Am J Physiol Lung Cell Mol Physiol 1997;273:L726-L732.
57. Arciniegas E, Frid MG, Douglas IS, Stenmark KR. Perspective on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2007;293:L1-L8. (Pubitemid 47080705)