Mesothelial- and epithelial-derived FGF9 have distinct functions in the regulation of lung development

Development

Volumn 138, Issue 15, 2011, Pages 3169-3177

  Yin, Yongjun ^a   Wang, Fen ^b   Ornitz, David M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

catenin; BMP4; Branching; FGF; FGF receptor; Lung; Mouse; Noggin; WNT

Indexed keywords

BETA CATENIN; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR; NOGGIN; WNT PROTEIN; WNT2 PROTEIN; WNT7B PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; LUNG HYPOPLASIA; MESOTHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; CARRIER PROTEINS; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EPITHELIUM; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 9; LUNG; MESODERM; MICE; ORGANOGENESIS; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WNT PROTEINS; WNT2 PROTEIN;

EID: 79960154778     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.065110     Document Type: Article

References (38)

1. Bellusci, S., Henderson, R., Winnier, G., Oikawa, T. and Hogan, B. L. (1996). Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122, 1693-1702.
2. Bellusci, S., Grindley, J., Emoto, H., Itoh, N. and Hogan, B. L. (1997). Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124, 4867-4878.
3. Chen, C., Ouyang, W., Grigura, V., Zhou, Q., Carnes, K., Lim, H., Zhao, G. Q., Arber, S., Kurpios, N., Murphy, T. L. et al. (2005). ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 436, 1030-1034.
4. Colvin, J. S., Feldman, B., Nadeau, J. H., Goldfarb, M. and Ornitz, D. M. (1999). Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev. Dyn. 216, 72-88.
5. Colvin, J. S., White, A., Pratt, S. J. and Ornitz, D. M. (2001a). Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128, 2095-2106.
6. Colvin, J. S., Green, R. P., Schmahl, J., Capel, B. and Ornitz, D. M. (2001b). Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104, 875-889.
7. De Langhe, S. P., Carraro, G., Tefft, D., Li, C., Xu, X., Chai, Y., Minoo, P., Hajihosseini, M. K., Drouin, J., Kaartinen, V. et al. (2008). Formation and differentiation of multiple mesenchymal lineages during lung development is regulated by beta-catenin signaling. PLoS ONE 3, e1516.
8. Dean, C. H., Miller, L. A., Smith, A. N., Dufort, D., Lang, R. A. and Niswander, L. A. (2005). Canonical Wnt signaling negatively regulates branching morphogenesis of the lung and lacrimal gland. Dev. Biol. 286, 270-286.
9. del Moral, P. M., De Langhe, S. P., Sala, F. G., Veltmaat, J. M., Tefft, D., Wang, K., Warburton, D. and Bellusci, S. (2006). Differential role of FGF9 on epithelium and mesenchyme in mouse embryonic lung. Dev. Biol. 293, 77-89.
10. Eblaghie, M. C., Reedy, M., Oliver, T., Mishina, Y. and Hogan, B. L. (2006). Evidence that autocrine signaling through Bmpr1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Dev. Biol. 291, 67-82.
11. Goss, A. M., Tian, Y., Tsukiyama, T., Cohen, E. D., Zhou, D., Lu, M. M., Yamaguchi, T. P. and Morrisey, E. E. (2009). Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Dev. Cell 17, 290-298.
12. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
13. Harris, K. S., Zhang, Z., McManus, M. T., Harfe, B. D. and Sun, X. (2006). Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. USA 103, 2208-2213.
14. Hendrix, N. D., Wu, R., Kuick, R., Schwartz, D. R., Fearon, E. R. and Cho, K. R. (2006). Fibroblast growth factor 9 has oncogenic activity and is a downstream target of Wnt signaling in ovarian endometrioid adenocarcinomas. Cancer Res. 66, 1354-1362.
15. Hyatt, B. A., Shangguan, X. and Shannon, J. M. (2002). BMP4 modulates fibroblast growth factor-mediated induction of proximal and distal lung differentiation in mouse embryonic tracheal epithelium in mesenchyme-free culture. Dev. Dyn. 225, 153-165.
16. Jang, C. W., Gao, L., Dickinson, M. E. and Behringer, R. R. (2010). Bmp4-directed nuclear cyan fluorescent protein provides a tool for live imaging and reveals cellular resolution of Bmp4 expression patterns during embryogenesis. Int. J. Dev. Biol. 54, 931-938.
17. Kratochwil, K., Dull, M., Fariñas, I., Galceran, J. and Grosschedl, R. (1996). Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev. 10, 1382-1394.
18. Levay-Young, B. K. and Navre, M. (1992). Growth and developmental regulation of wnt-2 (irp) gene in mesenchymal cells of fetal lung. Am. J. Physiol. 262, L672-L683.
19. Lin, Y., Liu, A., Zhang, S., Ruusunen, T., Kreidberg, J. A., Peltoketo, H., Drummond, I. and Vainio, S. (2001). Induction of ureter branching as a response to Wnt-2b signaling during early kidney organogenesis. Dev. Dyn. 222, 26-39.
20. Lin, Y., Liu, G. and Wang, F. (2006). Generation of an Fgf9 conditional null allele. Genesis 44, 150-154.
21. Mailleux, A. A., Tefft, D., Ndiaye, D., Itoh, N., Thiery, J. P., Warburton, D. and Bellusci, S. (2001). Evidence that SPROUTY2 functions as an inhibitor of mouse embryonic lung growth and morphogenesis. Mech. Dev. 102, 81-94.
22. Meijer, L., Skaltsounis, A. L., Magiatis, P., Polychronopoulos, P., Knockaert, M., Leost, M., Ryan, X. P., Vonica, C. A., Brivanlou, A., Dajani, R. et al. (2003). GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem. Biol. 10, 1255-1266.
23. Min, H., Danilenko, D. M., Scully, S. A., Bolon, B., Ring, B. D., Tarpley, J. E., DeRose, M. and Simonet, W. S. (1998). Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 12, 3156-3161.
24. Minowada, G., Jarvis, L. A., Chi, C. L., Neubuser, A., Sun, X., Hacohen, N., Krasnow, M. A. and Martin, G. R. (1999). Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126, 4465-4475.
25. Morrisey, E. E. and Hogan, B. L. (2010). Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev. Cell 18, 8-23.
26. Rajagopal, J., Carroll, T. J., Guseh, J. S., Bores, S. A., Blank, L. J., Anderson, W. J., Yu, J., Zhou, Q., McMahon, A. P. and Melton, D. A. (2008). Wnt7b stimulates embryonic lung growth by coordinately increasing the replication of epithelium and mesenchyme. Development 135, 1625-1634.
27. Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N. et al. (1999). Fgf10 is essential for limb and lung formation. Nat. Genet. 21, 138-141.
28. Shu, W., Jiang, Y. Q., Lu, M. M. and Morrisey, E. E. (2002). Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129, 4831-4842.
29. Sun, J., Chen, H., Chen, C., Whitsett, J. A., Mishina, Y., Bringas, P., Jr, Ma, J. C., Warburton, D. and Shi, W. (2008). Prenatal lung epithelial cell-specific abrogation of Alk3-bone morphogenetic protein signaling causes neonatal respiratory distress by disrupting distal airway formation. Am. J. Pathol. 172, 571-582.
30. Warburton, D., El-Hashash, A., Carraro, G., Tiozzo, C., Sala, F., Rogers, O., De Langhe, S., Kemp, P. J., Riccardi, D., Torday, J. et al. (2010). Lung organogenesis. Curr. Top. Dev. Biol. 90, 73-158.
31. Weaver, M., Yingling, J. M., Dunn, N. R., Bellusci, S. and Hogan, B. L. (1999). Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126, 4005-4015.
32. Weaver, M., Dunn, N. R. and Hogan, B. L. (2000). Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127, 2695-2704.
33. Weaver, M., Batts, L. and Hogan, B. L. (2003). Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev. Biol. 258, 169-184.
34. White, A. C., Xu, J., Yin, Y., Smith, C., Schmid, G. and Ornitz, D. M. (2006). FGF9 and SHH signaling coordinate lung growth and development through regulation of distinct mesenchymal domains. Development 133, 1507-1517.
35. White, A. C., Lavine, K. J. and Ornitz, D. M. (2007). FGF9 and SHH regulate mesenchymal Vegfa expression and development of the pulmonary capillary network. Development 134, 3743-3752.
36. Yi, L., Domyan, E. T., Lewandoski, M. and Sun, X. (2009). Fibroblast growth factor 9 signaling inhibits airway smooth muscle differentiation in mouse lung. Dev. Dyn. 238, 123-137.
37. Yin, Y., White, A. C., Huh, S. H., Hilton, M. J., Kanazawa, H., Long, F. and Ornitz, D. M. (2008). An FGF-WNT gene regulatory network controls lung mesenchyme development. Dev. Biol. 319, 426-436.
38. Yu, K., Xu, J., Liu, Z., Sosic, D., Shao, J., Olson, E. N., Towler, D. A. and Ornitz, D. M. (2003). Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130, 3063-3074.