Lens placode planar cell polarity is dependent on Cdc42-mediated junctional contraction inhibition

Developmental Biology

Volumn 412, Issue 1, 2016, Pages 32-43

  Muccioli, Maria ^a   Qaisi, Dalya ^a   Herman, Ken ^a   Plageman, Timothy F ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; F ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN CDC42; PROTEIN KINASE C; PROTEINASE ACTIVATED RECEPTOR; SHROOM3 PROTEIN; UNCLASSIFIED DRUG; CDC42 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CELL JUNCTION; CELL POLARITY; CONTROLLED STUDY; EMBRYO; FEMALE; GEOMETRY; IN VITRO STUDY; LENS EPITHELIUM; LENS EPITHELIUM CELL; LENS PLACODE; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; ANIMAL; CYTOLOGY; DOG; EMBRYOLOGY; LENS; MDCK CELL LINE; PHYSIOLOGY;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL POLARITY; DOGS; LENS, CRYSTALLINE; MADIN DARBY CANINE KIDNEY CELLS; MICE; MORPHOGENESIS;

EID: 84961603849     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.02.016     Document Type: Article

References (49)

1. Ashery-Padan R., Marquardt T., Zhou X., Gruss P. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes. Dev. 2000, 14:2701-2711.
2. Blankenship J.T., Backovic S.T., Sanny J.S., Weitz O., Zallen J.A. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 2006, 11:459-470.
3. Chauhan B., Plageman T., Lou M., Lang R. Epithelial morphogenesis: the mouse eye as a model system. Curr. Top. Dev. Biol. 2015, 111:375-399.
4. Chauhan B.K., Disanza A., Choi S.Y., Faber S.C., Lou M., Beggs H.E., Scita G., Zheng Y., Lang R.A. Cdc42- and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination. Development 2009, 136:3657-3667.
5. Chen L., Liao G., Yang L., Campbell K., Nakafuku M., Kuan C.Y., Zheng Y. Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc. Natl. Acad. Sci. USA 2006, 103:16520-16525.
6. 2+ signaling pathway. Dev. Biol. 2002, 244:342-357.
7. Eaton S., Wepf R., Simons K. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 1996, 135:1277-1289.
8. Elias B.C., Das A., Parekh D.V., Mernaugh G., Adams R., Yang Z., Brakebusch C., Pozzi A., Marciano D.K., Carroll T.J., Zent R. Cdc42 regulates epithelial cell polarity and cytoskeletal function during kidney tubule development. J. Cell Sci. 2015, 128:4293-4305.
9. Fagman H., Nilsson M. Morphogenesis of the thyroid gland. Mol. Cell Endocrinol. 2010, 323:35-54.
10. Fernandez-Gonzalez R., Simoes Sde M., Roper J.C., Eaton S., Zallen J.A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 2009, 17:736-743.
11. Fuhrmann S. Eye morphogenesis and patterning of the optic vesicle. Curr. Top. Dev. Biol. 2010, 93:61-84.
12. Harding M.J., McGraw H.F., Nechiporuk A. The roles and regulation of multicellular rosette structures during morphogenesis. Development 2014, 141:2549-2558.
13. Hendrix R., Madras N., Johnson R. Growth pressure can drive early chick lens geometries. Dev. Dyn. 1993, 196:153-164.
14. Hildebrand J.D. Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. J. Cell Sci. 2005, 118:5191-5203.
15. Hildebrand J.D., Soriano P. Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell 1999, 99:485-497.
16. Huang J., Rajagopal R., Liu Y., Dattilo L.K., Shaham O., Ashery-Padan R., Beebe D.C. The mechanism of lens placode formation: a case of matrix-mediated morphogenesis. Dev. Biol. 2011, 355:32-42.
17. Ishiuchi T., Takeichi M. Willin and Par3 cooperatively regulate epithelial apical constriction through aPKC-mediated ROCK phosphorylation. Nat. Cell Biol. 2011, 13:860-866.
18. Jidigam V.K., Gunhaga L. Development of cranial placodes: insights from studies in chick. Dev. Growth Differ. 2013, 55:79-95.
19. Jidigam V.K., Srinivasan R.C., Patthey C., Gunhaga L. Apical constriction and epithelial invagination are regulated by BMP activity. Biol. Open. 2015, 4:1782-1791.
20. Joberty G., Petersen C., Gao L., Macara I.G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2000, 2:531-539.
21. Kieserman E.K., Wallingford J.B. In vivo imaging reveals a role for Cdc42 in spindle positioning and planar orientation of cell divisions during vertebrate neural tube closure. J. Cell Sci. 2009, 122:2481-2490.
22. Kirjavainen A., Laos M., Anttonen T., Pirvola U. The Rho GTPase Cdc42 regulates hair cell planar polarity and cellular patterning in the developing cochlea. Biol. Open. 2015, 4:516-526.
23. Lang R.A., Herman K., Reynolds A.B., Hildebrand J.D., Plageman T.F. p120-catenin-dependent junctional recruitment of Shroom3 is required for apical constriction during lens pit morphogenesis. Development 2014, 141:3177-3187.
24. Lienkamp S.S., Liu K., Karner C.M., Carroll T.J., Ronneberger O., Wallingford J.B., Walz G. Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat. Genet. 2012, 44:1382-1387.
25. Liu X., Wang F., Wu H. Anisotropic growth of buckling-driven wrinkles in graphene monolayer. Nanotechnology 2015, 26:065701.
26. McGreevy E.M., Vijayraghavan D., Davidson L.A., Hildebrand J.D. Shroom3 functions downstream of planar cell polarity to regulate myosin II distribution and cellular organization during neural tube closure. Biol. Open. 2015, 4:186-196.
27. Mckeehan M.S. Cytological aspects of embryonic lens induction in the chick. J Exp. Zool. 1951, 117:31-64.
28. Murdoch J.N., Damrau C., Paudyal A., Bogani D., Wells S., Greene N.D., Stanier P., Copp A.J. Genetic interactions between planar cell polarity genes cause diverse neural tube defects in mice. Dis. Model. Mech. 2014, 7:1153-1163.
29. Nalbant P., Hodgson L., Kraynov V., Toutchkine A., Hahn K.M. Activation of endogenous Cdc42 visualized in living cells. Science 2004, 305:1615-1619.
30. Nishimura T., Takeichi M. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 2008, 135:1493-1502.
31. Pare A.C., Vichas A., Fincher C.T., Mirman Z., Farrell D.L., Mainieri A., Zallen J.A. A positional Toll receptor code directs convergent extension in Drosophila. Nature 2014, 515:523-527.
32. Plageman T.F., Chauhan B.K., Yang C., Jaudon F., Shang X., Zheng Y., Lou M., Debant A., Hildebrand J.D., Lang R.A. A Trio-RhoA-Shroom3 pathway is required for apical constriction and epithelial invagination. Development 2011, 138:5177-5188.
33. Plageman T.F., Chung M.I., Lou M., Smith A.N., Hildebrand J.D., Wallingford J.B., Lang R.A. Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination. Development 2010, 137:405-415.
34. Rajagopal R., Huang J., Dattilo L.K., Kaartinen V., Mishina Y., Deng C.X., Umans L., Zwijsen A., Roberts A.B., Beebe D.C. The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev. Biol. 2009, 335:305-316.
35. Sai X., Ladher R.K. Early steps in inner ear development: induction and morphogenesis of the otic placode. Front. Pharmacol. 2015, 6:19.
36. Scully K.M., Rosenfeld M.G. Pituitary development: regulatory codes in mammalian organogenesis. Science 2002, 295:2231-2235.
37. Simoes Sde M., Blankenship J.T., Weitz O., Farrell D.L., Tamada M., Fernandez-Gonzalez R., Zallen J.A. Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev. Cell 2010, 19:377-388.
38. Simoes Sde M., Mainieri A., Zallen J.A. Rho GTPase and Shroom direct planar polarized actomyosin contractility during convergent extension. J. Cell Biol. 2014, 204:575-589.
39. Snippert H.J., van der Flier L.G., Sato T., van Es J.H., van den Born M., Kroon-Veenboer C., Barker N., Klein A.M., van Rheenen J., Simons B.D., Clevers H. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143:134-144.
40. Tada M., Heisenberg C.P. Convergent extension: using collective cell migration and cell intercalation to shape embryos. Development 2012, 139:3897-3904.
41. Torban E., Patenaude A.M., Leclerc S., Rakowiecki S., Gauthier S., Andelfinger G., Epstein D.J., Gros P. Genetic interaction between members of the Vangl family causes neural tube defects in mice. Proc. Natl. Acad. Sci. USA 2008, 105:3449-3454.
42. Wald F.A., Oriolo A.S., Mashukova A., Fregien N.L., Langshaw A.H., Salas P.J. Atypical protein kinase C (iota) activates ezrin in the apical domain of intestinal epithelial cells. J. Cell Sci. 2008, 121:644-654.
43. Wallingford J.B. Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 2012, 28:627-653.
44. Wang Y., Guo N., Nathans J. The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J. Neurosci. 2006, 26:2147-2156.
45. Warner S.J., Longmore G.D. Cdc42 antagonizes Rho1 activity at adherens junctions to limit epithelial cell apical tension. J. Cell Biol. 2009, 187:119-133.
46. Welchman D.P., Mathies L.D., Ahringer J. Similar requirements for CDC-42 and the PAR-3/PAR-6/PKC-3 complex in diverse cell types. Dev. Biol. 2007, 305:347-357.
47. Williams M., Yen W., Lu X., Sutherland A. Distinct apical and basolateral mechanisms drive planar cell polarity-dependent convergent extension of the mouse neural plate. Dev. Cell 2014, 29:34-46.
48. Zallen J.A., Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell. 2004, 6:343-355.
49. Zwaan J., Pearce T.L. Cell population kinetics in the chicken lens primordium during and shortly after its contact with the optic cup. Dev. Biol. 1971, 25:96-118.