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Thread: Cytoskeletal Mechanisms During Animal Development (Current Topics in Developmental Bi

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    Post Cytoskeletal Mechanisms During Animal Development (Current Topics in Developmental Bi

    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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