Non-directional radial intercalation dominates deep cell behavior during zebrafish epiboly

被引:22
作者
Bensch, Robert [1 ,2 ]
Song, Sungmin [3 ,4 ]
Ronneberger, Olaf [1 ,2 ]
Driever, Wolfgang [2 ,3 ]
机构
[1] Univ Freiburg, Dept Comp Sci, D-79110 Freiburg, Germany
[2] Univ Freiburg, Ctr Biol Signalling Studies, BIOSS, D-79104 Freiburg, Germany
[3] Univ Freiburg, Fac Biol, Inst Biol 1, D-79104 Freiburg, Germany
[4] Univ Freiburg, Spemann Grad Sch Biol & Med, D-79104 Freiburg, Germany
来源
BIOLOGY OPEN | 2013年 / 2卷 / 08期
关键词
Gastrulation; Epiboly; Radial intercalation; Pou5f1;
D O I
10.1242/bio.20134614
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Epiboly is the first coordinated cell movement in most vertebrates and marks the onset of gastrulation. During zebrafish epiboly, enveloping layer (EVL) and deep cells spread over the vegetal yolk mass with a concomitant thinning of the deep cell layer. A prevailing model suggests that deep cell radial intercalations directed towards the EVL would drive deep cell epiboly. To test this model, we have globally recorded 3D cell trajectories for zebrafish blastomeres between sphere and 50% epiboly stages, and developed an image analysis framework to determine intercalation events, intercalation directionality, and migration speed for cells at specific positions within the embryo. This framework uses Voronoi diagrams to compute cell-to-cell contact areas, defines a feature-based spatio-temporal model for intercalation events and fits an anatomical coordinate system to the recorded datasets. We further investigate whether epiboly defects in MZspg mutant embryos devoid of Pou5f1/Oct4 may be caused by changes in intercalation behavior. In wild-type and mutant embryos, intercalations orthogonal to the EVL occur with no directional bias towards or away from the EVL, suggesting that there are no directional cues that would direct intercalations towards the EVL. Further, we find that intercalation direction is independent of the previous intercalation history of individual deep cells, arguing against cues that would program specific intrinsic directed migration behaviors. Our data support a dynamic model in which deep cells during epiboly migrate into space opening between the EVL and the yolk syncytial layer. Genetic programs determining cell motility may control deep cell dynamic behavior and epiboly progress. (C) 2013. Published by The Company of Biologists Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
引用
收藏
页码:845 / 854
页数:10
相关论文
共 20 条
  • [1] E-cadherin regulates cell movements and tissue formation in early zebrafish embryos
    Babb, SG
    Marrs, JA
    [J]. DEVELOPMENTAL DYNAMICS, 2004, 230 (02) : 263 - 277
  • [2] Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly
    Kane, DA
    McFarland, KN
    Warga, RM
    [J]. DEVELOPMENT, 2005, 132 (05): : 1105 - 1116
  • [3] Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy
    Keller, Philipp J.
    Schmidt, Annette D.
    Wittbrodt, Joachim
    Stelzer, Ernst H. K.
    [J]. SCIENCE, 2008, 322 (5904) : 1065 - 1069
  • [4] Cell migration during gastrulation
    Keller, R
    [J]. CURRENT OPINION IN CELL BIOLOGY, 2005, 17 (05) : 533 - 541
  • [5] How we are shaped: The biomechanics of gastrulation
    Keller, R
    Davidson, LA
    Shook, DR
    [J]. DIFFERENTIATION, 2003, 71 (03) : 171 - 205
  • [6] KELLER RE, 1980, J EMBRYOL EXP MORPH, V60, P201
  • [7] STAGES OF EMBRYONIC-DEVELOPMENT OF THE ZEBRAFISH
    KIMMEL, CB
    BALLARD, WW
    KIMMEL, SR
    ULLMANN, B
    SCHILLING, TF
    [J]. DEVELOPMENTAL DYNAMICS, 1995, 203 (03) : 253 - 310
  • [8] Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos
    Lachnit, Martina
    Kur, Esther
    Driever, Wolfgang
    [J]. DEVELOPMENTAL BIOLOGY, 2008, 315 (01) : 1 - 17
  • [9] Gastrulation movements: the logic and the nuts and bolts
    Leptin, M
    [J]. DEVELOPMENTAL CELL, 2005, 8 (03) : 305 - 320
  • [10] Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade
    Lunde, K
    Belting, HG
    Driever, W
    [J]. CURRENT BIOLOGY, 2004, 14 (01) : 48 - 55