Cytoskeletal Mechanisms During Animal Development (Current Topics in Developmental Biology) (Vol 31)
By David G. Capco (January 1996)
- Publisher: Academic Pr
- Number Of Pages: 501
- ISBN-10 / ASIN: 0121531317
- ISBN-13 / EAN: 9780121531317
Gametes, zygotes, and blastomeres of the embryo are cells and must exhibit
all of the functional characteristics of a cell in order to survive. In addition
to all the requisite cell functions, gametes, zygotes, and blastomeres of the
embryo face challenges posed by the developmental program that regulates
these cells. Gametes, zygotes, and embryos contain adaptations that allow
these specialized cells to meet and surmount the challenges posed by the
developmental program. These developmental challenges are directed at
the structure and function of these specialized cells, and consequently the
adaptations act through specializations in the cytoskeleton.
Many of these specializations in the cytoskeleton are most clearly detectable
at the time that these specialized cells undergo major remodeling of
structure and function, that is, at the time of a developmental transition.
Developmental transitions represent major partitions or landmarks in the
developmental program where the gametes, zygote, or blastomeres of the
embryo undergo a major structural and functional change. Several developmental
transitions are common to (or conserved among) all classes of
organisms, for example, gametogenesis, fertilization, and gastrulation. In
addition, there are typically developmental transitions specialized for
classes of organisms, for example, see Chapters 5 , 6, 9, and 10. These
transitions cause a radical change in cell function due to an underlying
remodeling of intracellular structure (or in the case of the multicellular
embryo both intracellular and intercellular remodeling result). This remodeling
alters the engineering of the cell, and as a consequence, the function
of the cell changes.
The chapters in this volume focus on the cytoskeletal specializations that
allow these cells to face and surmount the special developmental problems
unique to gametes, zygotes, and blastomeres of the embryo. In each of the
chapters readers will identify specializations of the cytoskeleton to meet
the challenges of the developmental program that exist at both conserved
and specialized developmental transitions. These cytoskeletal specializations
set gametes, zygotes, and blastomeres of the embryo apart from
somatic cells and also demonstrate remarkable adaptability in elements of
the cytoskeleton and in the elaboration of cytoskeletal structures.
Much of the current understanding of cytoskeletal organization and function
comes from analysis of results obtained from studies of somatic cells,
The somatic cells employed in many of these studies were obtained either
from cell lines maintained in vitro (e.g., 3T3 mouse fibroblasts, MDCK
cells, endothelial cell) or by explant from the organism (e.g., blood platelets,
macrophages, intestinal epithelium). From studies on such cells a minimum
of four roles for the cytoskeleton are generally accepted: (1) The cytoskeleton
provides the shape and infrastructural support for a cell as well as
positioning the organelles and nucleus. (2) Elements of the cytoskeleton
serve as “roadways” for the movement of cellular components, including
membranous elements, through the action of molecular motors. (3) The
cytoskeleton also positions both proteins and mRNA in nonrandom distributions
within cells, presumably at sites where such components are necessary.
(4) The cytoskeleton mediates cell motility.
The somatic cell types used to obtain the information outlined in the
previous paragraph are certainly important and central to the field of cell
biology. However, it must be recognized that there are limitations to the
type of knowledge obtained by analysis of somatic cells that can be applied
to the understanding of cells exhibiting specialized developmental roles.
These limitations exist at two levels. First, not all cells will survive under
in vitro culture conditions, and most that do lose their histotype. Even
those cells that are explanted from an organism and studied immediately,
such as intestinal epithelial cells, may retain their histotype, but may exhibit
a wound response that modifies the action of the cytoskeleton. Thus, while
results obtained from investigation of such cells certainly represent an
activity of the cytoskeleton within the cell’s repertoire, they may not representative
of the activity of the cell in its natural location or normal histotype.
Moreover, they may not be representative of cell types that cannot be
maintained for in vitro analysis even for short-term studies. Second, these
somatic cells do not face the special developmental challenges of gametes,
zygotes, and blastomeres of the embryo.
What are the special developmental challenges faced by gametes, zygotes,
and blastomeres and what adaptations exist to allow these special cells to
overcome the challenges? The answer to that question is the subject of this
volume. Some of these challenges will be common to all species, whereas
other challenges will be species-specific. The chapters in this volume present
these aspects for several classes of organisms. Any developmental biologist
could easily conceive of some of the challenges presented by the developmental
program that are conserved among different classes of organisms.
A few examples follow: (1) Oocytes, eggs, and blastomeres of the early
embryo contain an unusually large cytoplasmic volume compared to that
of somatic cells. This can present special problems in intracellular communication
when the cell must undergo a coordinated change, such as a progression
through the cell cycle in the case of blastomeres or a response of the
egg to the penetrating sperm. (2) The zygote is developmentally totipotent
through the elaboration of its developmental program. No somatic animal
cell is developmentally totipotent. (3) Fertilization requires cell fusion (i.e.,
between the egg and the sperm). In most species a mechanism exists to
permit entry of only one sperm. Typically, somatic cells do not fuse (this
statement excludes the terminal expression of a developmental program
in cell types such as muscle). Even when somatic cells are induced to fuse
through experimental manipulation, for example, to produce a hybridoma,
a totipotent zygote is not produced. (4) Fertilization requires the restoration
of ploidy through the unification of two different populations of chromosomes
without the loss of a chromosome or part of a chromosome. This
event occurs as pronuclear fusion or the unification of the two chromosomal
populations during M phase of the cell cycle. Fusion of somatic cells through
experimental manipulations usually results in the loss of one or more chromosomes
from the heterokaryon. (5) Eggs and blastomeres of embryos
exhibit unusual cell cycle regulation (i-e., specific cell cycle arrest points
for eggs and modified cell cycles for blastomeres). Typically, a somatic cell
is either progressing through the cell cycle (i.e., a stem cell) as is the case
for skin epithelial cells, or it is arrested late in Gapl of the cell cycle in a
state referred to Gapo. In the latter case, the cell cycle arrest point differs
from that of the egg, as does the mechanism of recusing the cell from Gap
(e.g., the cell cycle arrest in the egg is released by fusion with the sperm).
In the former case where the stem cell is progressing through the cell cycle,
the amount of time spent in Gap,, Gap2, and the synthesis phase (DNA
synthesis) for the stem cell is significantly longer than the times exhibited
by blastomeres of the embryo.
Several of the conserved modifications of cytoskeletal function that have
been identified in eggs, zygotes, and blastomeres address some of these
developmental challenges. Some examples follow: (1) To allow for rapid,
synchronized changes in large cells, such as the egg, cytoplasmic signal
transduction mechanisms are responsible for the rapid remodeling events
(of all parts of the egg including the cytoskeleton) at the developmental
transition that converts the egg into the zygote. (2) Where examined, microtubule
arrays appear to participate in the approximation of male and female
pronuclei within the egghygote cytoplasm, permitting syngamy to occur.
(3) Eggs contain extensive, cortical cytoskeletal domains that remodel as
a result of fertilization and perhaps permit exocytosis of cortical granules,
which provides the long-term block to polyspermy. (4) In those cases investigated,
the cortical cytoskeletal domain has been shown to be associated
(in some cases directly and in other cases indirectly) with components
capable of influencing the developmental fate of subsequently formed blastomeres.
(5) Developmental transitions are accompanied by a remodeling
of both the cortical and the internal cytoskeletal components, and in those
cases investigated the cytoskeletal remodeling has been shown to be regulated
by cytoplasmic signal transduction mechanisms.
The occurrences outlined in the previous paragraph, and other developmental
roles for the cytoskeleton, are presented in more detail in this
volume. The studies in this volume demonstrate a central role for the
cytoskeleton in development. Moreover, these studies demonstrate that
the cytoskeleton in eggs, zygotes, and blastomeres of the embryo is a
remarkably malleable structure. Even more remarkable is that the three
main filament networks (i.e., networks composed of actin filaments, microtubules,
and intermediate filaments) are capable of this vast array of specialized
activities. To date, no new filament network has been identified in
association with these special cellular functions during development, although
the existing cytoskeletal networks have been identified in highly
unusual aggregations and forms.
The cytoskeleton exhibits functions and activities in these specialized
cells that, to date, have no parallels in somatic cells. Yet all somatic cells
ultimately arise from the penetration of an egg by a sperm. Could it be
that these specialized activities of the cytoskeleton are involved only during
development and that once a somatic cell is formed the cytoskeleton no
longer can exhibit these special roles? Or could it be that our knowledge
of cytoskeletal function in somatic cells is skewed by the cell types available
to cell biologists for study? Let us look and wonder together.
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