Multi-scale quantification of tissue behavior during amniote embryo axis elongation

被引:47
作者
Benazeraf, Bertrand [1 ,2 ,3 ,11 ]
Beaupeux, Mathias [4 ]
Tchernookov, Martin [4 ]
Wallingford, Allison [2 ,3 ]
Salisbury, Tasha [2 ,3 ]
Shirtz, Amelia [2 ,3 ]
Shirtz, Andrew [5 ]
Huss, David [2 ,3 ,6 ]
Pourquie, Olivier [1 ,7 ,8 ,9 ]
Francois, Paul [4 ]
Lansford, Rusty [2 ,3 ,10 ]
机构
[1] Univ Strasbourg, IGBMC, UMR 7104, Dept Dev & Stem Cells,CNRS,Inserm,U964, F-67400 Illkirch Graffenstaden, France
[2] Childrens Hosp Los Angeles, Dept Radiol, Saban Res Inst, Los Angeles, CA 90027 USA
[3] Childrens Hosp Los Angeles, Dev Neurosci Program, Saban Res Inst, Los Angeles, CA 90027 USA
[4] McGill Univ, Dept Phys, Ernest Rutherford Phys Bldg,3600 Rue Univ, Montreal, PQ H3A 2T8, Canada
[5] Northern Michigan Univ, Comp Sci & Math Dept, Marquette, MI 49855 USA
[6] Univ Southern Calif, Dept Biol Sci, Los Angeles, CA 90089 USA
[7] Brigham & Womens Hosp, Dept Pathol, 60 Fenwood Rd, Boston, MA 02115 USA
[8] Harvard Med Sch, Dept Genet, 60 Fenwood Rd, Boston, MA 02115 USA
[9] Harvard Stem Cell Inst, 60 Fenwood Rd, Boston, MA 02115 USA
[10] Univ Southern Calif, Keck Sch Med, Dept Radiol Dev Stem Cells & Regenerat Med DSR, Los Angeles, CA 90033 USA
[11] Univ Toulouse, CNRS, CBD, CBI,UPS, Toulouse, France
来源
DEVELOPMENT | 2017年 / 144卷 / 23期
关键词
Confocal microscopy; Live imaging; Quail embryo; Axis elongation; Proliferation; PSM; Multi-tissue; Tissue deformations; Morphogenesis; CHICK-EMBRYO; XENOPUS-LAEVIS; CELL MOTILITY; BODY ELONGATION; POSTERIOR BODY; GASTRULATION; INTERCALATION; ZEBRAFISH; MESODERM; SEGMENTATION;
D O I
10.1242/dev.150557
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Embryonic axis elongation is a complex multi-tissue morphogenetic process responsible for the formation of the posterior part of the amniote body. How movements and growth are coordinated between the different posterior tissues (e.g. neural tube, axial and paraxial mesoderm, lateral plate, ectoderm, endoderm) to drive axis morphogenesis remain largely unknown. Here, we use quail embryos to quantify cell behavior and tissue movements during elongation. We quantify the tissue-specific contribution to axis elongation using 3D volumetric techniques, then quantify tissue-specific parameters such as cell density and proliferation. To study cell behavior at a multi-tissue scale, we used high-resolution 4D imaging of transgenic quail embryos expressing fluorescent proteins. We developed specific tracking and image analysis techniques to analyze cell motion and compute tissue deformations in 4D. This analysis reveals extensive sliding between tissues during axis extension. Further quantification of tissue tectonics showed patterns of rotations, contractions and expansions, which are consistent with the multi-tissue behavior observed previously. Our approach defines a quantitative and multi-scale method to analyze the coordination between tissue behaviors during early vertebrate embryo morphogenetic events.
引用
收藏
页码:4462 / 4472
页数:11
相关论文
共 44 条
[1]   Developmental stages of the Japanese quail [J].
Ainsworth, Sophie J. ;
Stanley, Rachael L. ;
Evans, Darrell J. R. .
JOURNAL OF ANATOMY, 2010, 216 (01) :3-15
[2]  
Araya C, 2016, DEV DYNAM, V245, P580, DOI [10.1002/DVDY.24401, 10.1002/dvdy.24401]
[3]  
Benazeraf B., 2017, DRYAD DIGITAL REPOSI, DOI [10.5061/dryad.4g1h2., DOI 10.5061/DRYAD.4G1H2]
[4]   A random cell motility gradient downstream of FGF controls elongation of an amniote embryo [J].
Benazeraf, Bertrand ;
Francois, Paul ;
Baker, Ruth E. ;
Denans, Nicolas ;
Little, Charles D. ;
Pourquie, Olivier .
NATURE, 2010, 466 (7303) :248-252
[5]  
Blanchard GB, 2009, NAT METHODS, V6, P458, DOI [10.1038/NMETH.1327, 10.1038/nmeth.1327]
[6]   Restricted expression of cdc25a in the tailbud is essential for formation of the zebrafish posterior body [J].
Bouldin, Cortney M. ;
Snelson, Corey D. ;
Farr, Gist H., III ;
Kimelman, David .
GENES & DEVELOPMENT, 2014, 28 (04) :384-395
[7]  
Chapman SC, 2001, DEV DYNAM, V220, P284, DOI 10.1002/1097-0177(20010301)220:3<284::AID-DVDY1102>3.3.CO
[8]  
2-X
[9]   Extracellular matrix dynamics during vertebrate axis formation [J].
Czirók, A ;
Rongish, BJ ;
Little, CD .
DEVELOPMENTAL BIOLOGY, 2004, 268 (01) :111-122
[10]   Control of the segmentation process by graded MAPK/ERK activation in the chick embryo [J].
Delfini, MC ;
Dubrulle, J ;
Malapert, P ;
Chal, J ;
Pourquié, O .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (32) :11343-11348