miR-17 family of microRNAs controls FGF10-mediated embryonic lung epithelial branching morphogenesis through MAPK14 and STAT3 regulation of E-Cadherin distribution

Developmental Biology

Volumn 333, Issue 2, 2009, Pages 238-250

  Carraro, Gianni ^a   El Hashash, Ahmed ^a   Guidolin, Diego ^b   Tiozzo, Caterina ^a   Turcatel, Gianluca ^a   Young, Brittany M ^a   De Langhe, Stijn P ^a   Bellusci, Saverio ^a   Shi, Wei ^a   Parnigotto, Pier Paolo ^b   Warburton, David ^a  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

E Cadherin; Lung; miRNAs; Structural homeostasis

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR RECEPTOR 2; MICRORNA; MICRORNA 106B; MICRORNA 17; MICRORNA 20A; MITOGEN ACTIVATED PROTEIN KINASE 14; STAT3 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE TARGETING; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; MOUSE; MULTIGENE FAMILY; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 69249221210     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.06.020     Document Type: Article

References (51)

1. Adachi-Yamada T., Nakamura M., Irie K., Tomoyasu Y., Sano Y., Mori E., Goto S., Ueno N., Nishida Y., and Matsumoto K. p38 mitogen-activated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis. Mol. Cell. Biol. 19 (1999) 2322-2329
2. Akao Y., Nakagawa Y., and Naoe T. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol. Pharm. Bull. 29 (2006) 903-906
3. Bellusci S., Henderson R., Winnier G., Oikawa T., and Hogan B.L. Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122 (1996) 1693-1702
4. Bellusci S., Grindley J., Emoto H., Itoh N., and Hogan B.L. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124 (1997) 4867-4878
5. Brennecke J., Hipfner D.R., Stark A., Russell R.B., and Cohen S.M. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113 (2003) 25-36
6. Bryant D.M., and Stow J.L. The ins and outs of E-cadherin trafficking. Trends Cell Biol. 14 (2004) 427-434
7. Cardoso W.V., and Lu J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 133 (2006) 1611-1624
8. Cloonan N., Brown M.K., Steptoe A.L., Wani S., Chan W.L., Forrest A.R., Kolle G., Gabrielli B., and Grimmond S.M. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol. 9 (2008) R127
9. Cohen S.M., Brennecke J., and Stark A. Denoising feedback loops by thresholding-a new role for microRNAs. Genes Dev. 20 (2006) 2769-2772
10. Conway G. STAT3-dependent pathfinding and control of axonal branching and target selection. Dev. Biol. 296 (2006) 119-136
11. Davis M.A., Ireton R.C., and Reynolds A.B. A core function for p120-catenin in cadherin turnover. J. Cell. Biol. 163 (2003) 525-534
12. De Langhe S.P., Sala F.G., Del Moral P.M., Fairbanks T.J., Yamada K.M., Warburton D., Burns R.C., and Bellusci S. Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev. Biol. 277 (2005) 316-331
13. Ding W., Shi W., Bellusci S., Groffen J., Heisterkamp N., Minoo P., and Warburton D. Sprouty2 downregulation plays a pivotal role in mediating crosstalk between TGF-beta1 signaling and EGF as well as FGF receptor tyrosine kinase-ERK pathways in mesenchymal cells. J. Cell. Physiol. 212 (2007) 796-806
14. Fish J.E., Santoro M.M., Morton S.U., Yu S., Yeh R.F., Wythe J.D., Ivey K.N., Bruneau B.G., Stainier D.Y., and Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 15 (2008) 272-284
15. Goomer R.S., Holst B.D., Wood I.C., Jones F.S., and Edelman G.M. Regulation in vitro of an L-CAM enhancer by homeobox genes HoxD9 and HNF-1. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 7985-7989
16. Guidolin D., Vacca A., Nussdorfer G.G., and Ribatti D. A new image analysis method based on topological and fractal parameters to evaluate the angiostatic activity of docetaxel by using the Matrigel assay in vitro. Microvasc.Res. 67 (2004) 117-124
17. Halbleib J.M., and Nelson W.J. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20 (2006) 3199-3214
18. Harris K.S., Zhang Z., McManus M.T., Harfe B.D., and Sun X. Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2208-2213
19. Hennig G., Lowrick O., Birchmeier W., and Behrens J. Mechanisms identified in the transcriptional control of epithelial gene expression. J. Biol. Chem. 271 (1996) 595-602
20. Hirai Y., Nose A., Kobayashi S., and Takeichi M. Expression and role of E- and P-cadherin adhesion molecules in embryonic histogenesis. II. Skin morphogenesis. Development 105 (1989) 271-277
21. Hogan B., Beddington R., Constantini F., and Lacy E. Manipulating the Mouse Embryo (1994), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
22. Hornstein E., Mansfield J.H., Yekta S., Hu J.K., Harfe B.D., McManus M.T., Baskerville S., Bartel D.P., and Tabin C.J. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 438 (2005) 671-674
23. Johnston R.J., and Hobert O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426 (2003) 845-849
24. Kida H., Mucenski M.L., Thitoff A.R., Le Cras T.D., Park K.S., Ikegami M., Muller W., and Whitsett J.A. GP130-STAT3 regulates epithelial cell migration and is required for repair of the bronchiolar epithelium. Am. J. Pathol. 172 (2008) 1542-1554
25. Kwon C., Han Z., Olson E.N., and Srivastava D. MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 18986-18991
26. Leckband D., and Prakasam A. Mechanism and dynamics of cadherin adhesion. Annu. Rev. Biomed. Eng. 8 (2006) 259-287
27. Liu Y., Martinez L., Ebine K., and Abe M.K. Role for mitogen-activated protein kinase p38 alpha in lung epithelial branching morphogenesis. Dev. Biol. 314 (2008) 224-235
28. Liu Y.N., Lee W.W., Wang C.Y., Chao T.H., Chen Y., and Chen J.H. Regulatory mechanisms controlling human E-cadherin gene expression. Oncogene. 24 (2005) 8277-8290
29. Lu Y., Thomson J.M., Wong H.Y., Hammond S.M., and Hogan B.L. Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev. Biol. 310 (2007) 442-453
30. Mathews D.H., Sabina J., Zuker M., and Turner D.H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288 (1999) 911-940
31. Mege R.M., Gavard J., and Lambert M. Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell. Biol. 18 (2006) 541-548
32. Palacios F., Schweitzer J.K., Boshans R.L., and D'Souza-Schorey C. ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4 (2002) 929-936
33. Palacios F., Tushir J.S., Fujita Y., and D'Souza-Schorey C. Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol. Cell. Biol. 25 (2005) 389-402
34. Park W.Y., Miranda B., Lebeche D., Hashimoto G., and Cardoso W.V. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev. Biol. 201 (1998) 125-134
35. Peinado H., Olmeda D., and Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 7 (2007) 415-428
36. Pepicelli C.V., Lewis P.M., and McMahon A.P. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr. Biol. 8 (1998) 1083-1086
37. Seul M., O'Gorman L., and Sammon M.J. Practical Algorithms for Image Analysis (2000), Cambridge Univ. Press, New York
38. Shi Y., Sawada J., Sui G., Affar el B., Whetstine J.R., Lan F., Ogawa H., Luke M.P., and Nakatani Y. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422 (2003) 735-738
39. Sokol N.S., and Ambros V. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev. 19 (2005) 2343-2354
40. Van Roy F., and Berx G. The cell-cell adhesion molecule E-cadherin. Cell. Mol. Life Sci. 65 (2008) 3756-3788
41. Ventura A., Young A.G., Winslow M.M., Lintault L., Meissner A., Erkeland S.J., Newman J., Bronson R.T., Crowley D., Stone J.R., Jaenisch R., Sharp P.A., and Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132 (2008) 875-886
42. Wang Z., Rose D.W., Hermanson O., Liu F., Herman T., Wu W., Szeto D., Gleiberman A., Krones A., Pratt K., Rosenfeld R., Glass C.K., and Rosenfeld M.G. Regulation of somatic growth by the p160 coactivator p/CIP. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13549-13554
43. Warburton D. Developmental biology: order in the lung. Nature 453 (2008) 733-735
44. Warburton D., Bellusci S., De Langhe S., Del Moral P.M., Fleury V., Mailleux A., Tefft D., Unbekandt M., Wang K., and Shi W. Molecular mechanisms of early lung specification and branching morphogenesis. Pediatr. Res. 57 (2005) 26R-37R
45. Weaver M., Dunn N.R., and Hogan B.L. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127 (2000) 2695-2704
46. Winnier G., Blessing M., Labosky P.A., and Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9 (1995) 2105-2116
47. Yamashita S., Miyagi C., Fukada T., Kagara N., Che Y.S., and Hirano T. Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 20 (2004) 298-302
48. Yap A.S., and Kovacs E.M. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell. Biol. 160 (2003) 11-16
49. Zhao Y., Samal E., and Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436 (2005) 214-220
50. Zohn I.E., Li Y., Skolnik E.Y., Anderson K.V., Han J., and Niswander L. p38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 125 (2006) 957-969
51. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415