Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo.

During development Caenorhabditis elegans changes from an embryo that is relatively spherical in shape to a long thin worm. This paper provides evidence that the elongation of the body is caused by the outermost layer of embryonic cells, the hypodermis, squeezing the embryo circumferentially. The hypodermal cells surround the embryo and are linked together by cellular junctions. Numerous circumferentially oriented bundles of microfilaments are present at the outer surfaces of the hypodermal cells as the embryo elongates. Elongation is associated with an apparent pressure on the internal cells of the embryo, and cytochalasin D reversibly inhibits both elongation and the increase in pressure. Circumferentially oriented microtubules also are associated with the outer membranes of the hypodermal cells during elongation. Experiments with the microtubule inhibitors colcemid, griseofulvin, and nocodazole suggest that the microtubules function to distribute across the membrane stresses resulting from microfilament contraction, such that the embryo decreases in circumference uniformly during elongation. While the cytoskeletal organization of the hypodermal cells appears to determine the shape of the embryo during elongation, an extracellular cuticle appears to maintain the body shape after elongation.

[1]  S. Brenner,et al.  Substoichiometric concentrations of cytochalasin D inhibit actin polymerization. Additional evidence for an F-actin treadmill. , 1979, The Journal of biological chemistry.

[2]  M D Flanagan,et al.  Cytochalasins block actin filament elongation by binding to high affinity sites associated with F-actin. , 1980, The Journal of biological chemistry.

[3]  D. Hirsh,et al.  Temperature-sensitive developmental mutants of Caenorhabditis elegans. , 1976, Developmental biology.

[4]  J. Tucker,et al.  Microtubules and control of insect egg shape , 1976, The Journal of cell biology.

[5]  T. E. Schroeder,et al.  Cytoplasmic filaments and morphogenetic movement in the amphibian neural tube. , 1967, Developmental biology.

[6]  W. Wood,et al.  Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos , 1983, Cell.

[7]  W. Wood,et al.  Parental effects and phenotypic characterization of mutations that affect early development in Caenorhabditis elegans. , 1980, Developmental biology.

[8]  J. Sulston,et al.  Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. , 1977, Developmental biology.

[9]  S. Brenner The genetics of Caenorhabditis elegans. , 1974, Genetics.

[10]  E. Wulf,et al.  Fluorescent phallotoxin, a tool for the visualization of cellular actin. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[11]  K. Weber,et al.  Interaction of griseofulvin with microtubules, microtubule protein and tubulin. , 1977, Journal of molecular biology.

[12]  J. Sulston,et al.  The embryonic cell lineage of the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[13]  R. Edgar,et al.  Cuticle of Caenorhabditis elegans: its isolation and partial characterization , 1981, The Journal of cell biology.

[14]  S. Ochoa,et al.  Enzymatic synthesis of polynucleotides. II. Distribution of polynucleotide phosphorylase. , 1957, The Journal of biological chemistry.

[15]  J. Harris,et al.  Structure and Function in the Nematodes: Internal Pressure and Cuticular Structure in Ascaris , 1957 .

[16]  D. Albertson Formation of the first cleavage spindle in nematode embryos. , 1984, Developmental biology.

[17]  S. Tanenbaum Cytochalasins. Biochemical and cell biological aspects. , 1978 .

[18]  J. Kilmartin,et al.  Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line , 1982, The Journal of cell biology.

[19]  D. Mayer,et al.  Preparation of tetramethylrhodaminyl-phalloidin and uptake of the toxin into short-term cultured hepatocytes by endocytosis. , 1983, Experimental cell research.

[20]  S. Granett,et al.  Ultrastructural localization of the high molecular weight proteins associated with in vitro-assembled brain microtubules , 1975, The Journal of cell biology.

[21]  S. Ward,et al.  Electron microscopical reconstruction of the anterior sensory anatomy of the nematode caenorhabditis elegans , 1975, The Journal of comparative neurology.

[22]  L. Staehelin,et al.  Structure and function of intercellular junctions. , 1974, International review of cytology.

[23]  J. Sulston,et al.  Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. , 1980, Developmental biology.

[24]  T. E. Schroeder,et al.  Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy. , 1970, Journal of embryology and experimental morphology.

[25]  O. Glaser On the mechanism of morphological differentiation in the nervous system. I. The transformation of a neural plate into a neural tube , 1914 .

[26]  Walter Birchmeier,et al.  Stress fiber sarcomeres of fibroblasts are contractile , 1980, Cell.

[27]  B. Burnside,et al.  Microtubules and microfilaments in newt neuralation. , 1971, Developmental biology.

[28]  A G Jacobson,et al.  Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. , 1976, The Journal of experimental zoology.

[29]  B. Burnside Microtubules and Microfilaments in Amphibian Neurulation , 1973 .

[30]  M. Schliwa Proteins associated with cytoplasmic actin , 1981, Cell.

[31]  E. Schierenberg,et al.  Cell lineages and developmental defects of temperature-sensitive embryonic arrest mutants in Caenorhabditis elegans. , 1980, Developmental biology.

[32]  P. Alberch,et al.  The mechanical basis of morphogenesis. I. Epithelial folding and invagination. , 1981, Developmental biology.

[33]  D. Went Oocyte maturation without follicular epithelium alters egg shape in a dipteran insect , 1978 .

[34]  D. Hirsh,et al.  Segregation of germline granules in early embryos of Caenorhabditis elegans: an electron microscopic analysis. , 1983, Journal of embryology and experimental morphology.