Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling

被引:233
作者
Nishimura, Tamako [1 ]
Takeichi, Masatoshi [1 ]
机构
[1] RIKEN, Ctr Dev Biol, Chuo Ku, Kobe, Hyogo 6500047, Japan
来源
DEVELOPMENT | 2008年 / 135卷 / 08期
关键词
shroom; rho kinase; myosin; neural tube; epithelial remodeling; chicken; MDCK cells; mouse;
D O I
10.1242/dev.019646
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Remodeling of epithelial sheets plays important roles in animal morphogenesis. Shroom3 is known to regulate the apical constriction of epithelial cells. Here, we show that Shroom3 binds ROCKs and recruits them to the epithelial apical junctions. We identified the Shroom3- binding site (RII-C1) on ROCKs, and found that RII-C1 could antagonize the Shroom3- ROCK interaction, interfering with the action of Shroom3 on cell morphology. In the invaginating neural plate/tube, Shroom3 colocalized with ROCKs at the apical junctions; Shroom3 depletion or RII-C1 expression in the tube removed these apically localized ROCKs, and concomitantly blocked neural tube closure. Closing neural plate exhibited peculiar cell assemblies, including rosette formation, as well as a planar-polarized distribution of phosphorylated myosin regulatory light chain, but these were abolished by ROCK inhibition or RII-C1 expression. These results demonstrate that the Shroom3- ROCK interaction is crucial for the regulation of epithelial and neuroepithelial cell arrangement and remodeling.
引用
收藏
页码:1493 / 1502
页数:10
相关论文
共 36 条
[1]   Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase) [J].
Amano, M ;
Ito, M ;
Kimura, K ;
Fukata, Y ;
Chihara, K ;
Nakano, T ;
Matsuura, Y ;
Kaibuchi, K .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1996, 271 (34) :20246-20249
[2]   The rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation [J].
Barrett, K ;
Leptin, M ;
Settleman, J .
CELL, 1997, 91 (07) :905-915
[3]   Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation [J].
Bertet, C ;
Sulak, L ;
Lecuit, T .
NATURE, 2004, 429 (6992) :667-671
[4]   Multicellular rosette formation links planar cell polarity to tissue morphogenesis [J].
Blankenship, J. Todd ;
Backovic, Stephanie T. ;
Sanny, Justina S. P. ;
Weitz, Ori ;
Zallen, Jennifer A. .
DEVELOPMENTAL CELL, 2006, 11 (04) :459-470
[5]   The genetic basis of mammalian neurulation [J].
Copp, AJ ;
Greene, NDE ;
Murdoch, JN .
NATURE REVIEWS GENETICS, 2003, 4 (10) :784-793
[6]   A PUTATIVE CELL SIGNAL ENCODED BY THE FOLDED GASTRULATION GENE COORDINATES CELL-SHAPE CHANGES DURING DROSOPHILA GASTRULATION [J].
COSTA, M ;
WILSON, ET ;
WIESCHAUS, E .
CELL, 1994, 76 (06) :1075-1089
[7]   Differential actin-dependent localization modulates the evolutionarily conserved activity of Shroom family proteins [J].
Dietz, Megan L. ;
Bernaciak, Teresa M. ;
Vendetti, Frank ;
Kielec, Joseph M. ;
Hildebrand, Jeffrey D. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2006, 281 (29) :20542-20554
[8]   Shroom2, a myosin-VIIa-and actin-binding protein, directly interacts with ZO-1 at tight junctions [J].
Etournay, Raphael ;
Zwaenepoel, Ingrid ;
Perfettini, Isabelle ;
Legrain, Pierre ;
Petit, Christine ;
El-Amraoui, Aziz .
JOURNAL OF CELL SCIENCE, 2007, 120 (16) :2838-2850
[9]   Shroom2 (APXL) regulates melanosome biogenesis and localization in the retinal pigment epithelium [J].
Fairbank, Pamela D. ;
Lee, Chanjae ;
Ellis, Avegiyel ;
Hildebrand, Jeffrey D. ;
Gross, Jeffrey M. ;
Wallingford, John B. .
DEVELOPMENT, 2006, 133 (20) :4109-4118
[10]   JUNCTIONAL COMPLEXES IN VARIOUS EPITHELIA [J].
FARQUHAR, MG ;
PALADE, GE .
JOURNAL OF CELL BIOLOGY, 1963, 17 (02) :375-&