Cell rearrangements, cell divisions and cell death in a migrating epithelial sheet in the abdomen of Drosophila

被引:45
作者
Bischoff, Marcus [1 ,2 ]
Cseresnyes, Zoltan [1 ]
机构
[1] Univ Cambridge, Dept Zool, Cambridge CB2 3EJ, England
[2] MRC Lab Mol Biol, Cambridge CB2 0QH, England
来源
DEVELOPMENT | 2009年 / 136卷 / 14期
基金
英国医学研究理事会; 英国惠康基金;
关键词
Morphogenesis; Cell migration; Cell division orientation; MYOSIN-II; DORSAL CLOSURE; MORPHOGENESIS; POLARITY; INTERCALATION; GASTRULATION; HEDGEHOG; METAMORPHOSIS; EMBRYOGENESIS; ORIENTATION;
D O I
10.1242/dev.035410
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
During morphogenesis, cell movements, cell divisions and cell death work together to form complex patterns and to shape organs. These events are the outcome of decisions made by many individual cells, but how these decisions are controlled and coordinated is elusive. The adult abdominal epidermis of Drosophila is formed during metamorphosis by divisions and extensive cell migrations of the diploid histoblasts, which replace the polyploid larval cells. Using in vivo 4D microscopy, we have studied the behaviour of the histoblasts and analysed in detail how they reach their final position and to what extent they rearrange during their spreading. Tracking individual cells, we show that the cells migrate in two phases that differ in speed, direction and amount of cellular rearrangement. Cells of the anterior (A) and posterior (P) compartments differ in their behaviour. Cells near the A/P border are more likely to change their neighbours during migration. The mitoses do not show any preferential orientation. After mitosis, the sisters become preferentially aligned with the direction of movement. Thus, in the abdomen, it is the extensive cell migrations that appear to contribute most to morphogenesis. This contrasts with other developing epithelia, such as the wing imaginal disc and the embryonic germband in Drosophila, where oriented mitoses and local cell rearrangements appear to direct morphogenesis. Furthermore, our results suggest that an active force created by the histoblasts contributes to the formation of the adult epidermis. Finally, we show that histoblasts occasionally undergo apoptosis.
引用
收藏
页码:2403 / 2411
页数:9
相关论文
共 41 条
[31]  
Oda H, 2001, J CELL SCI, V114, P493
[32]   REGULATION AND METAMORPHOSIS OF THE ABDOMINAL HISTOBLASTS OF DROSOPHILA-MELANOGASTER [J].
ROSELAND, CR ;
SCHNEIDERMAN, HA .
WILHELM ROUXS ARCHIVES OF DEVELOPMENTAL BIOLOGY, 1979, 186 (03) :235-265
[33]   Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos:: its role in nuclear axial expansion and its regulation by Cdc2 activity [J].
Royou, A ;
Sullivan, W ;
Karess, R .
JOURNAL OF CELL BIOLOGY, 2002, 158 (01) :127-137
[34]   Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: Variability of development and regional specification [J].
Schnabel, R ;
Hutter, H ;
Moerman, D ;
Schnabel, H .
DEVELOPMENTAL BIOLOGY, 1997, 184 (02) :234-265
[35]   Global cell sorting in the C-elegans embryo defines a new mechanism for pattern formation [J].
Schnabel, R ;
Bischoff, M ;
Hintze, A ;
Schulz, AK ;
Hejnol, A ;
Meinhardt, H ;
Hutter, H .
DEVELOPMENTAL BIOLOGY, 2006, 294 (02) :418-431
[36]   ORGANIZING ACTIVITY OF WINGLESS PROTEIN IN DROSOPHILA [J].
STRUHL, G ;
BASLER, K .
CELL, 1993, 72 (04) :527-540
[37]  
Struhl G, 1997, DEVELOPMENT, V124, P2143
[38]   A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis [J].
Tawk, Marcel ;
Araya, Claudio ;
Lyons, Dave A. ;
Reugels, Alexander M. ;
Girdler, Gemma C. ;
Bayley, Philippa R. ;
Hyde, David R. ;
Tada, Masazumi ;
Clarke, Jonathan D. W. .
NATURE, 2007, 446 (7137) :797-800
[39]   Apoptotic force and tissue dynamics during Drosophila embryogenesis [J].
Toyama, Yusuke ;
Peralta, Xomalin G. ;
Wells, Adrienne R. ;
Kiehart, Daniel P. ;
Edwards, Glenn S. .
SCIENCE, 2008, 321 (5896) :1683-1686
[40]   The amniote primitive streak is defined by epithelial cell intercalation before gastrulation [J].
Voiculescu, Octavian ;
Bertocchini, Federica ;
Wolpert, Lewis ;
Keller, Ray E. ;
Stern, Claudio D. .
NATURE, 2007, 449 (7165) :1049-1052