Epithelial cell division in the Xenopus laevis embryo
during gastrulation
GUILLAUME HATTE
1,2
, MARC TRAMIER
1,2
, CLAUDE PRIGENT
1,2
and JEAN-PIERRE TASSAN*
,1,2
1
CNRS UMR 6290 and
2
Université de Rennes 1, Institut de Génétique et Développement de Rennes,
Rennes, France
ABSTRACT How vertebrate epithelial cells divide in vivo and how the cellular environment influ-
ences cell division is currently poorly understood. A sine qua non condition to study cell division in
situ is the ease of observation of cell division.This is fulfilled in the Xenopus embryo at the gastrula
stage where polarized epithelial cells divide with a high frequency at the surface of the organism.
Recently, using this model system, we have shown that epithelial cells divide by asymmetric fur-
rowing and that the mode of cell division is regulated during development. Here, we further char-
acterize epithelial cell division in situ. To this end, we used confocal microscopy to study epithelial
cell division in the ectoderm of the Xenopus laevis gastrula. Cell division was followed either by
indirect immunofluorescence in fixed embryos or by live imaging of embryos transiently expressing
diverse fluorescent proteins. Here, we show that during cytokinesis, the plasma membranes of the
two daughter cells are usually separated by a gap. For most divisions, daughter cells make contacts
basally at a distance from the furrow tip which creates an inverted teardrop-like shaped volume
tightly associated with the furrow. At the end of cytokinesis, the inverted teardrop is resorbed;
thus it is a transient structure. Several proteins involved in cytokinesis are localized at the tip of
the inverted teardrop suggesting that the formation of the gap could be an active process. We also
show that intercalation of neighboring cells between daughter cells occasionally occurs during
cytokinesis. Our results reveal an additional level of complexity in the relationship between dividing
cells and also with their neighboring cells during cytokinesis in the Xenopus embryo epithelium.
KEY WORDS: cytokinesis, asymmetric furrowing, contractile ring, anillin, actin, myosin
Introduction
Cytokinesis is the process by which dividing cells separate to
produce two daughter cells. It is driven by a contractile ring com-
posed of actin and myosin. It is commonly accepted that this ring
is established perpendicularly to the mitotic spindle and is placed
at equidistance of the mitotic chromosomes allowing their equal
distribution to two daughter cells (Almonacid and Paoletti, 2010,
Rappaport, 1996). The precise spatio-temporal regulation of the
ring ensures the proper cell separation which otherwise could
ultimately lead to abortive cytokinesis (Normand and King, 2010).
Although a detailed mechanism of action is currently unknown, it is
established that the actomyosin-based contractile ring produces the
force necessary for ingression of the plasma membrane between
the two daughter cells (Fededa and Gerlich, 2012). In addition to
actin and myosin, multiple proteins are necessary to cytokinesis to
Int. J. Dev. Biol. 58: 775-781 (2014)
doi: 10.1387/ijdb.140277jt
www.intjdevbiol.com
*Address correspondence to: Jean-Pierre Tassan. IGDR, UMR 6290 CNRS Univ Rennes 1, 2 avenue du Professeur Léon Bernard, 35043 Rennes Cedex, France.
E-mail: jean-pierre.tassan@univ-rennes1.fr
Supplementary Material (3 movies and 3 igures) for this paper is available at: http://dx.doi.org/10.1387/ijdb.140277jt
Accepted: 7 December 2014
ISSN: Online 1696-3547, Print 0214-6282
© 2014 UBC Press
Printed in Spain
Abbreviations used in this paper: MHC, myosin II heavy chain.
proceed (Green et al., 2012). Anillin, a large multidomain protein
is involved in the spatial positioning of the cleavage furrow during
cytokinesis (Piekny and Maddox, 2010). Various anillin domains
allow its interaction with cytokinetic proteins including actin, myosin
and septin. In absence of anillin, the cytokinetic ring still forms,
however it is not stably positioned. In isolated in vitro unpolarized
cultured cells, the contraction of the contractile ring appears ap-
proximately concentric.
Vertebrate cell division is mostly studied in in vitro cultured
cells. For example, isolated cells are particularly well suited for
high-throughput screen (Kittler et al., 2004). Although, studies
using the in vitro cultured cells have led to the discovery of basic
mechanisms governing cytokinesis, it appears paradoxical that the
majority of information on cell division of multicellular organisms