Dynamic Fgf signaling couples morphogenesis and migration in the zebrafish lateral line primordium

被引:180
作者
Lecaudey, Virginie [1 ]
Cakan-Akdogan, Gulcin [1 ]
Norton, William H. J. [2 ]
Gilmour, Darren [1 ]
机构
[1] European Mol Biol Lab, Heidelberg, Germany
[2] GSF Res Ctr Environm & Hlth, Inst Dev Genet, Munich, Germany
来源
DEVELOPMENT | 2008年 / 135卷 / 16期
关键词
lateral line primordium; zebrafish; collective migration; Fgf; rosette morphogenesis;
D O I
10.1242/dev.025981
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
The collective migration of cells in the form of cohesive tissues is a hallmark of both morphogenesis and repair. The extrinsic cues that direct these complex migrations usually act by regulating the dynamics of a specific subset of cells, those at the leading edge. Given that normally the function of tissue migration is to lay down multicellular structures, such as branched epithelial networks or sensory organs, it is surprising how little is known about the mechanisms that organize cells behind the leading edge. Cells of the zebrafish lateral line primordium switch from mesenchyme-like leader cells to epithelial rosettes that develop into mechanosensory organs. Here, we show that this transition is regulated by an Fgf signaling circuit that is active within the migrating primordium. Point sources of Fgf ligand drive surrounding cells towards a 'non-leader' fate by increasing their epithelial character, a prerequisite for rosette formation. We demonstrate that the dynamic expression of Fgf ligands determines the spatiotemporal pattern of epithelialization underlying sensory organ formation in the lateral line. Furthermore, this work uncovers a surprising link between internal tissue organization and collective migration.
引用
收藏
页码:2695 / 2705
页数:11
相关论文
共 46 条
[1]   Signaling to cytoskeletal dynamics during chemotaxis [J].
Affolter, M ;
Weijer, CJ .
DEVELOPMENTAL CELL, 2005, 9 (01) :19-34
[2]   FGF-dependent Notch signaling maintains the spinal cord stem zone [J].
Akai, J ;
Halley, PA ;
Storey, KG .
GENES & DEVELOPMENT, 2005, 19 (23) :2877-2887
[3]   A clock and wavefront mechanism for somite formation [J].
Baker, RE ;
Schnell, S ;
Maini, PK .
DEVELOPMENTAL BIOLOGY, 2006, 293 (01) :116-126
[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]   Epithelial cell adhesion in the developing Drosophila retina is regulated by Atonal and the EGF receptor pathway [J].
Brown, Katherine E. ;
Baonza, Antonio ;
Freeman, Matthew .
DEVELOPMENTAL BIOLOGY, 2006, 300 (02) :710-721
[6]   Distinct roles for two receptor tyrosine kinases in epithelial branching morphogenesis in Drosophila [J].
Cabernard, C ;
Affolter, M .
DEVELOPMENTAL CELL, 2005, 9 (06) :831-842
[7]   FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak [J].
Ciruna, B ;
Rossant, J .
DEVELOPMENTAL CELL, 2001, 1 (01) :37-49
[8]   Molecular basis of cell migration in the fish lateral line:: Role of the chemokine receptor CXCR4 and of its ligand, SDF1 [J].
David, NB ;
Sapède, D ;
Saint-Etienne, L ;
Thisse, C ;
Thisse, B ;
Dambly-Chaudière, C ;
Rosa, FM ;
Ghysen, A .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (25) :16297-16302
[9]   fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo [J].
Dubrulle, J ;
Pourquié, O .
NATURE, 2004, 427 (6973) :419-422
[10]   FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation [J].
Dubrulle, J ;
McGrew, MJ ;
Pourquié, O .
CELL, 2001, 106 (02) :219-232