CFTR and Wnt/beta-catenin signaling in lung development
Tóm tắt
Cystic fibrosis transmembrane conductance regulator (CFTR) was shown previously to modify stretch induced differentiation in the lung. The mechanism for CFTR modulation of lung development was examined by in utero gene transfer of either a sense or antisense construct to alter CFTR expression levels. The BAT-gal transgenic reporter mouse line, expressing β-galactosidase under a canonical Wnt/β-catenin-responsive promoter, was used to assess the relative roles of CFTR, Wnt, and parathyroid hormone-related peptide (PTHrP) in lung organogenesis. Adenoviruses containing full-length CFTR, a short anti-sense CFTR gene fragment, or a reporter gene as control were used in an intra-amniotic gene therapy procedure to transiently modify CFTR expression in the fetal lung. A direct correlation between CFTR expression levels and PTHrP levels was found. An inverse correlation between CFTR and Wnt signaling activities was demonstrated. These data are consistent with CFTR participating in the mechanicosensory process essential to regulate Wnt/β-Catenin signaling required for lung organogenesis.
Tài liệu tham khảo
Featherstone NC, Jesudason EC, Connell MG, Fernig DG, Wray S, Losty PD, Burdyga TV: Spontaneous propagating calcium waves underpin airway peristalsis in embryonic rat lung. American journal of respiratory cell and molecular biology. 2005, 33 (2): 153-160. 10.1165/rcmb.2005-0137OC.
Featherstone NC, Connell MG, Fernig DG, Wray S, Burdyga TV, Losty PD, Jesudason EC: Airway smooth muscle dysfunction precedes teratogenic congenital diaphragmatic hernia and may contribute to hypoplastic lung morphogenesis. American journal of respiratory cell and molecular biology. 2006, 35 (5): 571-578. 10.1165/rcmb.2006-0079OC.
Ingber DE: Cellular mechanotransduction: putting all the pieces together again. Faseb J. 2006, 20 (7): 811-827. 10.1096/fj.05-5424rev.
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. The Journal of biological chemistry. 2003, 278 (41): 40231-40238. 10.1074/jbc.M305892200.
Vogel V: Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annual review of biophysics and biomolecular structure. 2006, 35: 459-488. 10.1146/annurev.biophys.35.040405.102013.
Haga JH, Li YS, Chien S: Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells. Journal of biomechanics. 2007, 40 (5): 947-960. 10.1016/j.jbiomech.2006.04.011.
Cohen JC, Larson JE: Cystic fibrosis transmembrane conductance regulator (CFTR) dependent cytoskeletal tension during lung organogenesis. Dev Dyn. 2006, 235 (10): 2736-2748. 10.1002/dvdy.20912.
Cohen JC, Scott D, Miller J, Zhang J, Zhou P, Larson JE: Transient in utero knockout (TIUKO) of C-MYC affects late lung and intestinal development in the mouse. BMC developmental biology. 2004, 4: 4-10.1186/1471-213X-4-4.
Cardoso WV, Lu J: Regulation of early lung morphogenesis: questions, facts and controversies. Development (Cambridge, England). 2006, 133 (9): 1611-1624.
Sekhon HS, Keller JA, Proskocil BJ, Martin EL, Spindel ER: Maternal nicotine exposure upregulates collagen gene expression in fetal monkey lung. Association with alpha7 nicotinic acetylcholine receptors. Am J Respir Cell Mol Biol. 2002, 26 (1): 31-41.
Larson JE, Morrow SL, Delcarpio JB, Bohm RP, Ratterree MS, Blanchard JL, Cohen JC: Gene transfer into the fetal primate: evidence for the secretion of transgene product. Mol Ther. 2000, 2 (6): 631-639. 10.1006/mthe.2000.0209.
Larson JE, Delcarpio JB, Farberman MM, Morrow SL, Cohen JC: CFTR modulates lung secretory cell proliferation and differentiation. Am J Physiol Lung Cell Mol Physiol. 2000, 279 (2): L333-41.
Morrow SL, Larson JE, Nelson S, Sekhon HS, Ren T, Cohen JC: Modification of development by the CFTR gene in utero. Molecular genetics and metabolism. 1998, 65 (3): 203-212. 10.1006/mgme.1998.2755.
Larson JE, Morrow SL, Happel L, Sharp JF, Cohen JC: Reversal of cystic fibrosis phenotype in mice by gene therapy in utero. Lancet. 1997, 349 (9052): 619-620. 10.1016/S0140-6736(05)61567-X.
Cohen JC, Morrow SL, Cork RJ, Delcarpio JB, Larson JE: Molecular pathophysiology of cystic fibrosis based on the rescued knockout mouse model. Molecular genetics and metabolism. 1998, 64 (2): 108-118. 10.1006/mgme.1998.2683.
Larson JE, Cohen JC: Improvement of pulmonary hypoplasia associated with congenital diaphragmatic hernia by in utero CFTR gene therapy. Am J Physiol Lung Cell Mol Physiol. 2006, 291 (1): L4-10. 10.1152/ajplung.00372.2005.
Rehan VK, Torday JS: Exploiting the PTHrP signaling pathway to treat chronic lung disease. Drugs Today (Barc). 2007, 43 (5): 317-331. 10.1358/dot.2007.43.5.1062665.
Torday JS, Rehan VK: Developmental cell/molecular biologic approach to the etiology and treatment of bronchopulmonary dysplasia. Pediatric research. 2007, 62 (1): 2-7. 10.1203/PDR.0b013e31806772a1.
Torday JS, Rehan VK: Up-regulation of fetal rat lung parathyroid hormone-related protein gene regulatory network down-regulates the Sonic Hedgehog/Wnt/betacatenin gene regulatory network. Pediatric research. 2006, 60 (4): 382-388. 10.1203/01.pdr.0000238326.42590.03.
Torday JS: Parathyroid hormone-related protein is a gravisensor in lung and bone cell biology. Adv Space Res. 2003, 32 (8): 1569-1576. 10.1016/S0273-1177(03)90397-8.
Echelard Y, Vassileva G, McMahon AP: Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development (Cambridge, England). 1994, 120 (8): 2213-2224.
Sekhon HS, Larson JE: In utero gene transfer into the pulmonary epithelium. Nat Med. 1995, 1 (11): 1201-1203. 10.1038/nm1195-1201.
Garrett DJ, Larson JE, Dunn D, Marrero L, Cohen JC: In utero recombinant adeno-associated virus gene transfer in mice, rats, and primates. BMC Biotechnol. 2003, 3 (1): 16-10.1186/1472-6750-3-16.
Cohen JC, Larson JE: Pathophysiologic consequences following inhibition of a CFTR-dependent developmental cascade in the lung. BMC developmental biology. 2005, 5 (1): 2-10.1186/1471-213X-5-2.
Torday JS, Rehan VK: The evolutionary continuum from lung development to homeostasis and repair. American journal of physiology. 2007, 292 (3): L608-11.
Broackes-Carter FC, Mouchel N, Gill D, Hyde S, Bassett J, Harris A: Temporal regulation of CFTR expression during ovine lung development: implications for CF gene therapy. Human molecular genetics. 2002, 11 (2): 125-131. 10.1093/hmg/11.2.125.
Marcorelles P, Montier T, Gillet D, Lagarde N, Ferec C: Evolution of CFTR protein distribution in lung tissue from normal and CF human fetuses. Pediatric pulmonology. 2007, 42 (11): 1032-1040. 10.1002/ppul.20690.
Sanchez-Esteban J, Tsai SW, Sang J, Qin J, Torday JS, Rubin LP: Effects of mechanical forces on lung-specific gene expression. The American journal of the medical sciences. 1998, 316 (3): 200-204. 10.1097/00000441-199809000-00009.
Larson JE, Cohen JC: Improvement of Pulmonary Hypoplasia Associated with Congenital Diaphragmatic Hernia by In Utero CFTR Gene Therapy. Am J Physiol Lung Cell Mol Physiol. 2006
Torday JS, Sanchez-Esteban J, Rubin LP: Paracrine mediators of mechanotransduction in lung development. The American journal of the medical sciences. 1998, 316 (3): 205-208. 10.1097/00000441-199809000-00010.
Rehan VK, Dargan-Batra SK, Wang Y, Cerny L, Sakurai R, Santos J, Beloosesky R, Gayle D, Torday JS: A paradoxical temporal response of the PTHrP/PPARgamma signaling pathway to lipopolysaccharide in an in vitro model of the developing rat lung. American journal of physiology. 2007, 293 (1): L182-90.
Rehan VK, Sakurai R, Wang Y, Santos J, Huynh K, Torday JS: Reversal of nicotine-induced alveolar lipofibroblast-to-myofibroblast transdifferentiation by stimulants of parathyroid hormone-related protein signaling. Lung. 2007, 185 (3): 151-159. 10.1007/s00408-007-9007-0.
Rehan VK, Sugano S, Wang Y, Santos J, Romero S, Dasgupta C, Keane MP, Stahlman MT, Torday JS: Evidence for the presence of lipofibroblasts in human lung. Experimental lung research. 2006, 32 (8): 379-393. 10.1080/01902140600880257.
Moore KA, Polte T, Huang S, Shi B, Alsberg E, Sunday ME, Ingber DE: Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn. 2005, 232 (2): 268-281. 10.1002/dvdy.20237.
Sheridan MB, Fong P, Groman JD, Conrad C, Flume P, Diaz R, Harris C, Knowles M, Cutting GR: Mutations in the beta-subunit of the epithelial Na+ channel in patients with a cystic fibrosis-like syndrome. Human molecular genetics. 2005, 14 (22): 3493-3498. 10.1093/hmg/ddi374.
Tavernarakis N, Driscoll M: Mechanotransduction in Caenorhabditis elegans: the role of DEG/ENaC ion channels. Cell biochemistry and biophysics. 2001, 35 (1): 1-18. 10.1385/CBB:35:1:01.
Treharne KJ, Crawford RM, Xu Z, Chen JH, Best OG, Schulte EA, Gruenert DC, Wilson SM, Sheppard DN, Kunzelmann K, Mehta A: Protein kinase CK2, cystic fibrosis transmembrane conductance regulator, and the deltaF508 mutation: F508 deletion disrupts a kinase-binding site. The Journal of biological chemistry. 2007, 282 (14): 10804-10813. 10.1074/jbc.M610956200.
Chasan B, Geisse NA, Pedatella K, Wooster DG, Teintze M, Carattino MD, Goldmann WH, Cantiello HF: Evidence for direct interaction between actin and the cystic fibrosis transmembrane conductance regulator. Eur Biophys J. 2002, 30 (8): 617-624. 10.1007/s00249-001-0188-9.
Cantiello HF: Role of actin filament organization in CFTR activation. Pflugers Arch. 2001, 443 Suppl 1: S75-80.
Borthwick LA, McGaw J, Conner G, Taylor CJ, Gerke V, Mehta A, Robson L, Muimo R: The formation of the cAMP/protein kinase A-dependent annexin 2 S100A10 complex with cystic fibrosis conductance regulator protein (CFTR) regulates CFTR channel function. Molecular biology of the cell. 2007, 18 (9): 3388-3397. 10.1091/mbc.E07-02-0126.
Jarvinen E, Salazar-Ciudad I, Birchmeier W, Taketo MM, Jernvall J, Thesleff I: Continuous tooth generation in mouse is induced by activated epithelial Wnt/beta-catenin signaling. Proceedings of the National Academy of Sciences of the United States of America. 2006, 103 (49): 18627-18632. 10.1073/pnas.0607289103.