Filopodial-Tension Model of Convergent-Extension of Tissues

被引:19
作者
Belmonte, Julio M. [1 ,2 ,4 ]
Swat, Maciej H. [1 ,2 ]
Glazier, James A. [1 ,3 ]
机构
[1] Indiana Univ Bloomington, Biocomplex Inst, Bloomington, IN 47405 USA
[2] Indiana Univ Bloomington, Dept Phys, Bloomington, IN 47405 USA
[3] Indiana Univ Bloomington, Dept Intelligent Syst Engn, Bloomington, IN USA
[4] EMBL, Dev Biol DB Unit, Heidelberg, Germany
基金
英国工程与自然科学研究理事会;
关键词
CELL INTERCALATION; FORCE PRODUCTION; XENOPUS-LAEVIS; GASTRULATION; REARRANGEMENT; MOTILITY; POLARITY; INVAGINATION; MECHANISMS; SIMULATION;
D O I
10.1371/journal.pcbi.1004952
中图分类号
Q5 [生物化学];
学科分类号
071010 ; 081704 ;
摘要
In convergent-extension (CE), a planar-polarized epithelial tissue elongates (extends) in-plane in one direction while shortening (converging) in the perpendicular in-plane direction, with the cells both elongating and intercalating along the converging axis. CE occurs during the development of most multicellular organisms. Current CE models assume cell or tissue asymmetry, but neglect the preferential filopodial activity along the convergent axis observed in many tissues. We propose a cell-based CE model based on asymmetric filopodial tension forces between cells and investigate how cell-level filopodial interactions drive tissue-level CE. The final tissue geometry depends on the balance between external rounding forces and cell-intercalation traction. Filopodial-tension CE is robust to relatively high levels of planar cell polarity misalignment and to the presence of non-active cells. Addition of a simple mechanical feedback between cells fully rescues and even improves CE of tissues with high levels of polarity misalignments. Our model extends easily to three dimensions, with either one converging and two extending axes, or two converging and one extending axes, producing distinct tissue morphologies, as observed in vivo.
引用
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页数:20
相关论文
共 44 条
[1]   An intracellular partitioning-based framework for tissue cell polarity in plants and animals [J].
Abley, Katie ;
de Reuille, Pierre Barbier ;
Strutt, David ;
Bangham, Andrew ;
Prusinkiewicz, Przemyslaw ;
Maree, Athanasius F. M. ;
Grieneisen, Veronica A. ;
Coen, Enrico .
DEVELOPMENT, 2013, 140 (10) :2061-2074
[2]   Convergent extension by intercalation without mediolaterally fixed cell motion [J].
Backes, Tracy M. ;
Latterman, Russell ;
Small, Stephen A. ;
Mattis, Steven ;
Pauley, Gwyn ;
Reilly, Emily ;
Lubkin, Sharon R. .
JOURNAL OF THEORETICAL BIOLOGY, 2009, 256 (02) :180-186
[3]   RhoA regulates initiation of invagination, but not convergent extension, during sea urchin gastrulation [J].
Beane, WS ;
Gross, JM ;
McClay, DR .
DEVELOPMENTAL BIOLOGY, 2006, 292 (01) :213-225
[4]   Gastrulation in amphibian embryos, regarded as a succession of biomechanical feedback events [J].
Beloussov, LV ;
Luchinskaya, NN ;
Ermakov, AS ;
Glagoleva, NS .
INTERNATIONAL JOURNAL OF DEVELOPMENTAL BIOLOGY, 2006, 50 (2-3) :113-122
[5]   Tip-1 induces filopodia growth and is important for gastrulation movements during zebrafish development [J].
Besser, Jaya ;
Leito, Jelani T. D. ;
van der Meer, David L. M. ;
Bagowski, Christoph P. .
DEVELOPMENT GROWTH & DIFFERENTIATION, 2007, 49 (03) :205-214
[6]   The Role of Spatially Controlled Cell Proliferation in Limb Bud Morphogenesis [J].
Boehm, Bernd ;
Westerberg, Henrik ;
Lesnicar-Pucko, Gaja ;
Raja, Sahdia ;
Rautschka, Michael ;
Cotterell, James ;
Swoger, Jim ;
Sharpe, James .
PLOS BIOLOGY, 2010, 8 (07)
[7]   How Filopodia Pull: What We Know About the Mechanics and Dynamics of Filopodia [J].
Bornschloegl, Thomas .
CYTOSKELETON, 2013, 70 (10) :590-603
[8]   Do lamellipodia have the mechanical capacity to drive convergent extension? [J].
Brodland, GW .
INTERNATIONAL JOURNAL OF DEVELOPMENTAL BIOLOGY, 2006, 50 (2-3) :151-155
[9]  
Davidson LA, 1999, DEVELOPMENT, V126, P4547
[10]   Integrin α5β1 and fibronectin regulate polarized cell protrusions required for Xenopus convergence and extension [J].
Davidson, Lance A. ;
Marsden, Mungo ;
Keller, Raymond ;
DeSimone, Douglas W. .
CURRENT BIOLOGY, 2006, 16 (09) :833-844