A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration

Nature Genetics

Volumn 40, Issue 7, 2008, Pages 862-870

  Zhang, Yuzhen ^a   Goss, Ashley M ^a   Cohen, Ethan David ^a   Kadzik, Rachel ^a   Lepore, John J ^a   Muthukumaraswamy, Karthika ^a   Yang, Jifu ^a   DeMayo, Francesco J ^b   Whitsett, Jeffrey A ^c   Parmacek, Michael S ^a   Morrisey, Edward E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; TRANSCRIPTION FACTOR GATA 6; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL REGENERATION; DOWN REGULATION; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL EXPANSION;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; FRIZZLED RECEPTORS; GATA6 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; LUNG; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, G-PROTEIN-COUPLED; REGENERATION; RESPIRATORY MUCOSA; RESPIRATORY PHYSIOLOGY; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS;

EID: 46249127489     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.157     Document Type: Article

References (49)

1. Cardoso, W.V. Molecular regulation of lung development. Annu. Rev. Physiol. 63, 471-494 (2001).
2. Cardoso, W.V. & Lu, J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 133, 1611-1624 (2006).
3. Minoo, P., Su, G., Drum, H., Bringas, P. & Kimura, S. Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev. Biol. 209, 60-71 (1999).
4. Wan, H. et al. Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. J. Biol. Chem. 280, 13809-13816 (2005).
5. Yang, H., Lu, M.M., Zhang, L., Whitsett, J.A. & Morrisey, E.E. GATA6 regulates differentiation of distal lung epithelium. Development 129, 2233-2246 (2002).
6. Blenkinsopp, W.K. Proliferation of respiratory tract epithelium in the rat. Exp. Cell Res. 46, 144-154 (1967).
7. Giangreco, A., Reynolds, S.D. & Stripp, B.R. Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am. J. Pathol. 161, 173-182 (2002).
8. Rawlins, E.L. & Hogan, B.L. Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133, 2455-2465 (2006).
9. Kim, C.F. et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835 (2005).
10. Zhang, Y. et al. GATA and Nkx factors synergistically regulate tissue-specific gene expression and development in vivo. Development 134, 189-198 (2007).
11. Lepore, J.J. et al. GATA-6 regulates semaphorin 3C and is required in cardiac neural crest for cardiovascular morphogenesis. J. Clin. Invest. 116, 929-939 (2006).
12. Shu, W. et al. Wnt/β-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-distal patterning in the lung. Dev. Biol. 283, 226-239 (2005).
13. Perl, A.K., Tichelaar, J.W. & Whitsett, J.A. Conditional gene expression in the respiratory epithelium of the mouse. Transgenic Res. 11, 21-29 (2002).
14. Tichelaar, J.W., Lu, W. & Whitsett, J.A. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J. Biol. Chem. 275, 11858-11864 (2000).
15. Li, H., Malbon, C.C. & Wang, H.Y. Gene profiling of Frizzled-1 and Frizzled-2 signaling: expression of G-protein-coupled receptor chimeras in mouse F9 teratocarcinoma embryonal cells. Mol. Pharmacol. 65, 45-55 (2004).
16. 2+ pathway to antagonize Wnt/β-catenin signaling. Mol. Cell. Biol. 23, 131-139 (2003).
17. Topol, L. et al. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J. Cell Biol. 162, 899-908 (2003).
18. Torres, M.A. et al. Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J. Cell Biol. 133, 1123-1137 (1996).
19. Cohen, E.D. et al. Wnt/β-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J. Clin. Invest. 117, 1794-1804 (2007).
20. Yokoyama, H., Ogino, H., Stoick-Cooper, C.L., Grainger, R.M. & Moon, R.T. Wnt/β-catenin signaling has an essential role in the initiation of limb regeneration. Dev. Biol. 306, 170-178 (2007).
21. Stoick-Cooper, C.L. et al. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134, 479-489 (2007).
22. Fathke, C. et al. Wnt signaling induces epithelial differentiation during cutaneous wound healing. BMC Cell Biol. 7, 4 (2006).
23. Maretto, S. et al. Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304 (2003).
24. Plopper, C.G., Suverkropp, C., Morin, D., Nishio, S. & Buckpitt, A. Relationship of cytochrome P-450 activity to Clara cell cytotoxicity. I. Histopathologic comparison of the respiratory tract of mice, rats and hamsters after parenteral administration of naphthalene. J. Pharmacol. Exp. Ther. 261, 353-363 (1992).
25. Harada, N. et al. Intestinal polyposis in mice with a dominant stable mutation of the β-catenin gene. EMBO J. 18, 5931-5942 (1999).
26. Iwanaga, K. et al. Pten inactivation accelerates oncogenic K-ras-initiated tumorigenesis in a mouse model of lung cancer. Cancer Res. 68, 1119-1127 (2008).
27. Yin, Z. et al. Hop functions downstream of Nkx2.1 and GATA6 to mediate HDAC-dependent negative regulation of pulmonary gene expression. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L191-L199 (2006).
28. Liu, C., Morrisey, E.E. & Whitsett, J.A. GATA-6 is required for maturation of the lung in late gestation. Am. J. Physiol. Lung Cell. Mol. Physiol. 283, L468-L475 (2002).
29. Weidenfeld, J., Shu, W., Zhang, L., Millar, S.E. & Morrisey, E.E. The WNT7b promoter is regulated by TTF-1, GATA6, and Foxa2 in lung epithelium. J. Biol. Chem. 277, 21061-21070 (2002).
30. Bruno, M.D., Korfhagen, T.R., Liu, C., Morrisey, E.E. & Whitsett, J.A. GATA-6 activates transcription of surfactant protein A. J. Biol. Chem. 275, 1043-1049 (2000).
31. Ahumada, A. et al. Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 298, 2006-2010 (2002).
32. 2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161, 769-777 (2003).
33. 2+/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275, 12701-12711 (2000).
34. Mucenski, M.L. et al. Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L971-L979 (2005).
35. Okubo, T. & Hogan, B.L. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol. 3, 11 (2004).
36. Chazaud, C., Yamanaka, Y., Pawson, T. & Rossant, J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624 (2006).
37. Morrisey, E.E. et al. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 12, 3579-3590 (1998).
38. Ralston, A. & Rossant, J. Genetic regulation of stem cell origins in the mouse embryo. Clin. Genet. 68, 106-112 (2005).
39. Lin, L. et al. Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc. Natl. Acad. Sci. USA 104, 9313-9318 (2007).
40. Besson, A. et al. Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype. Genes Dev. 21, 1731-1746 (2007).
41. Davé, V. et al. Conditional deletion of Pten causes bronchiolar hyperplasia. Am. J. Respir. Cell Mol. Biol. 38, 337-345 (2007).
42. Ventura, J.J. et al. p38α MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat. Genet. 39, 750-758 (2007).
43. Yanagi, S. et al. Pten controls lung morphogenesis, bronchioalveolar stem cells, and onset of lung adenocarcinomas in mice. J. Clin. Invest. 117, 2929-2940 (2007).
44. Brault, V. et al. Inactivation of the β-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264 (2001).
45. Iwanaga, K. et al. Pten inactivation accelerates oncogenic K-ras-initiated tumorigenesis in a mouse model of lung cancer. Cancer Res. 68, 1119-1127 (2008).
46. Morrisey, E.E., Ip, H.S., Lu, M.M. & Parmacek, M.S. GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev. Biol. 177, 309-322 (1996).
47. Shu, W., Jiang, Y.Q., Lu, M.M. & Morrisey, E.E. Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129, 4831-4842 (2002).
48. Lepore, J.J., Cappola, T.P., Mericko, P.A., Morrisey, E.E. & Parmacek, M.S. GATA-6 regulates genes promoting synthetic functions in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 25, 309-314 (2005).
49. Shu, W., Yang, H., Zhang, L., Lu, M.M. & Morrisey, E.E. Characterization of a new subfamily of winged-helix/forkhead (Fox) genes that are expressed in the lung and act as transcriptional repressors. J. Biol. Chem. 276, 27488-27497 (2001).