Cadherin-6B stimulates an epithelial mesenchymal transition and the delamination of cells from the neural ectoderm via LIMK/cofilin mediated non-canonical BMP receptor signaling

Developmental Biology

Volumn 366, Issue 2, 2012, Pages 232-243

  Park, Ki Sook ^a,b   Gumbiner, Barry M ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Kyung Hee University   (South Korea)

Author keywords

BMP; Cadherin 6B; Cofilin; EMT; LIMK; Neural crest; Non canonical

Indexed keywords

ACTIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CADHERIN; CADHERIN 6B; COFILIN; LIM KINASE; SMAD PROTEIN; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL DELAMINATION; CHICKEN; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME MECHANISM; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIZATION; MUTATION; NEURAL CREST; NEURAL TUBE; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 84861222173     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.04.005     Document Type: Article

References (39)

1. Adams C.L., Nelson W.J., Smith S.J. Quantitative analysis of cadherin-catenin-actin reorganization during development of cell-cell adhesion. J. Cell Biol. 1996, 135:1899-1911.
2. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998, 393:805-809.
3. Bravo-Cordero J.J., Oser M., Chen X., Eddy R., Hodgson L., Condeelis J. A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr. Biol. 2011, 21:635-644.
4. Chan M.C., Nguyen P.H., Davis B.N., Ohoka N., Hayashi H., Du K., Lagna G., Hata A. A novel regulatory mechanism of the bone morphogenetic protein (BMP) signaling pathway involving the carboxyl-terminal tail domain of BMP type II receptor. Mol. Cell Biol. 2007, 27:5776-5789.
5. Chen X., Macara I.G. Par-3 mediates the inhibition of LIM kinase 2 to regulate cofilin phosphorylation and tight junction assembly. J. Cell Biol. 2006, 172:671-678.
6. Cheung M., Briscoe J. Neural crest development is regulated by the transcription factor Sox9. Development 2003, 130:5681-5693.
7. Cheung M., Chaboissier M.C., Mynett A., Hirst E., Schedl A., Briscoe J. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 2005, 8:179-192.
8. Coles E.G., Taneyhill L.A., Bronner-Fraser M. A critical role for Cadherin6B in regulating avian neural crest emigration. Dev. Biol. 2007, 312:533-544.
9. Derynck R., Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425:577-584.
10. Foletta V.C., Lim M.A., Soosairajah J., Kelly A.P., Stanley E.G., Shannon M., He W., Das S., Massague J., Bernard O. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 2003, 162:1089-1098.
11. Foletta V.C., Moussi N., Sarmiere P.D., Bamburg J.R., Bernard O. LIM kinase 1, a key regulator of actin dynamics, is widely expressed in embryonic and adult tissues. Exp. Cell Res. 2004, 294:392-405.
12. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
13. Gurniak C.B., Perlas E., Witke W. The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Dev. Biol. 2005, 278:231-241.
14. Hassel S., Eichner A., Yakymovych M., Hellman U., Knaus P., Souchelnytskyi S. Proteins associated with type II bone morphogenetic protein receptor (BMPR-II) and identified by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2004, 4:1346-1358.
15. Kavsak P., Rasmussen R.K., Causing C.G., Bonni S., Zhu H., Thomsen G.H., Wrana J.L. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell 2000, 6:1365-1375.
16. Kwiatkowski A.V., Maiden S.L., Pokutta S., Choi H.J., Benjamin J.M., Lynch A.M., Nelson W.J., Weis W.I., Hardin J. In vitro and in vivo reconstitution of the cadherin-catenin-actin complex from Caenorhabditis elegans. Proc. Natl. Acad. Sci. U S A 2010, 107:14591-14596.
17. Lee-Hoeflich S.T., Causing C.G., Podkowa M., Zhao X., Wrana J.L., Attisano L. Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J. 2004, 23:4792-4801.
18. Lin C.W., Yen S.T., Chang H.T., Chen S.J., Lai S.L., Liu Y.C., Chan T.H., Liao W.L., Lee S.J. Loss of cofilin 1 disturbs actin dynamics, adhesion between enveloping and deep cell layers and cell movements during gastrulation in zebrafish. PLoS One 2010, 5:e15331.
19. Liu J.P., Jessell T.M. A role for rhoB in the delamination of neural crest cells from the dorsal neural tube. Development 1998, 125:5055-5067.
20. Massague J. TGFbeta in cancer. Cell 2008, 134:215-230.
21. Miyazono K., Kamiya Y., Morikawa M. Bone morphogenetic protein receptors and signal transduction. J. Biochem. 2010, 147:35-51.
22. Mouneimne G., DesMarais V., Sidani M., Scemes E., Wang W., Song X., Eddy R., Condeelis J. Spatial and temporal control of cofilin activity is required for directional sensing during chemotaxis. Curr. Biol. 2006, 16:2193-2205.
23. Nagumo Y., Han J., Bellila A., Isoda H., Tanaka T. Cofilin mediates tight-junction opening by redistributing actin and tight-junction proteins. Biochem. Biophys. Res. Commun. 2008, 377:921-925.
24. Nishihara A., Watabe T., Imamura T., Miyazono K. Functional heterogeneity of bone morphogenetic protein receptor-II mutants found in patients with primary pulmonary hypertension. Mol. Biol. Cell 2002, 13:3055-3063.
25. Ozdamar B., Bose R., Barrios-Rodiles M., Wang H.R., Zhang Y., Wrana J.L. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 2005, 307:1603-1609.
26. Park K.S., Gumbiner B.M. Cadherin 6B induces BMP signaling and de-epithelialization during the epithelial mesenchymal transition of the neural crest. Development 2010, 137:2691-2701.
27. Patel S.D., Ciatto C., Chen C.P., Bahna F., Rajebhosale M., Arkus N., Schieren I., Jessell T.M., Honig B., Price S.R., Shapiro L. Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 2006, 124:1255-1268.
28. Perez-Moreno M., Jamora C., Fuchs E. Sticky business: orchestrating cellular signals at adherens junctions. Cell 2003, 112:535-548.
29. Podkowa M., Zhao X., Chow C.W., Coffey E.T., Davis R.J., Attisano L. Microtubule stabilization by bone morphogenetic protein receptor-mediated scaffolding of c-Jun N-terminal kinase promotes dendrite formation. Mol. Cell. Biol. 2010, 30:2241-2250.
30. Rosenzweig B.L., Imamura T., Okadome T., Cox G.N., Yamashita H., ten Dijke P., Heldin C.H., Miyazono K. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. U S A 1995, 92:7632-7636.
31. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
32. Shoval I., Ludwig A., Kalcheim C. Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 2007, 134:491-501.
33. Taneyhill L.A., Coles E.G., Bronner-Fraser M. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development 2007, 134:1481-1490.
34. Timmer J.R., Wang C., Niswander L. BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors. Development 2002, 129:2459-2472.
35. Wang W., Eddy R., Condeelis J. The cofilin pathway in breast cancer invasion and metastasis. Nat. Rev. Cancer 2007, 7:429-440.
36. Wong W.K., Knowles J.A., Morse J.H. Bone morphogenetic protein receptor type II C-terminus interacts with c-Src: implication for a role in pulmonary arterial hypertension. Am. J. Respir. Cell Mol. Biol. 2005, 33:438-446.
37. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
38. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 1998, 393:809-812.
39. Zhang L., Luo J., Wan P., Wu J., Laski F., Chen J. Regulation of cofilin phosphorylation and asymmetry in collective cell migration during morphogenesis. Development 2011, 138:455-464.