Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans

C. Elegans has four muscle quadrants that are used for locomotion. Contraction is converted to locomotion because muscle cells are anchored to the cuticle (the outer covering of the worm) by a specialized basement membrane and hemidesmosome structures in the hypodermis (a cellular syncytium that covers the worm and secretes the cuticle). To study muscle assembly, we have used antibodies to determine the spatial and temporal distribution of muscle and attachment structure components in wild-type and mutant C. elegans embryos. Myofibrillar components are first observed diffusely distributed in the muscle cells, and are expressed in some dividing cells. Later, the components accumulate at the membrane adjacent to the hypodermis where the sarcomeres will form, showing that the cells have become polarized. Assembly of muscle attachment structures is spatially and temporally coordinated with muscle assembly suggesting that important developmental signals may be passed between muscle and hypodermal cells. Analysis of embryos homozygous for mutations that affect muscle assembly show that muscle components closer to the membrane than the affected protein assemble quite well, while those further from the membrane do not. Our results suggest a model where lattice assembly is initiated at the membrane and the spatial organization of the structural elements of the muscle is dictated by membrane proximal events, not by the filament components themselves.

[1]  S. Tapscott,et al.  Taxol induces postmitotic myoblasts to assemble interdigitating microtubule-myosin arrays that exclude actin filaments , 1981, The Journal of cell biology.

[2]  J. Murray,et al.  Polygons and adhesion plaques and the disassembly and assembly of myofibrils in cardiac myocytes , 1989, The Journal of cell biology.

[3]  L. Tskhovrebova,et al.  Electron microscopic study of ?-actinin , 1975 .

[4]  K. Weber,et al.  Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts , 1986, The Journal of cell biology.

[5]  R. Waterston,et al.  Dominant mutations affecting muscle structure in Caenorhabditis elegans that map near the actin gene cluster. , 1984, Journal of molecular biology.

[6]  J. Trinick Understanding the functions of titin and nebulin , 1992, FEBS letters.

[7]  S. Ebashi,et al.  α-Actinin, a New Structural Protein from Striated Muscle , 1965 .

[8]  S. Labeit,et al.  Towards a molecular understanding of titin. , 1992, The EMBO journal.

[9]  S. Craig,et al.  Cap Z06132), a Barbed End Actin-capping Protein, Is a Component of the Z-line of Skeletal Muscle Materials and Methods , 1987 .

[10]  Richard O. Hynes,et al.  Integrins: Versatility, modulation, and signaling in cell adhesion , 1992, Cell.

[11]  T. Wright,et al.  The phenogenetics of the embryonic mutant, lethal myospheroid, in Drosophila melanogaster. , 1960, The Journal of experimental zoology.

[12]  C. Fyrberg,et al.  Perturbations of Drosophila alpha-actinin cause muscle paralysis, weakness, and atrophy but do not confer obvious nonmuscle phenotypes , 1992, The Journal of cell biology.

[13]  D. Fischman AN ELECTRON MICROSCOPE STUDY OF MYOFIBRIL FORMATION IN EMBRYONIC CHICK SKELETAL MUSCLE , 1967, The Journal of cell biology.

[14]  S. M. Wang,et al.  Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin , 1988, The Journal of cell biology.

[15]  H. F. Epstein,et al.  Paramyosin is necessary for determination of nematode thick filament length in vivo , 1980, Cell.

[16]  D. Riddle,et al.  Fine structure of the Caenorhabditis elegans secretory-excretory system. , 1983, Journal of ultrastructure research.

[17]  R. Waterston,et al.  The minor myosin heavy chain, mhcA, of Caenorhabditis elegans is necessary for the initiation of thick filament assembly. , 1989, The EMBO journal.

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

[19]  Y. Toyama,et al.  Effects of taxol and Colcemid on myofibrillogenesis. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[20]  T Masaki,et al.  Differential distribution of subsets of myofibrillar proteins in cardiac nonstriated and striated myofibrils , 1990, The Journal of cell biology.

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

[22]  S. Ebashi,et al.  Alpha-actinin, a new structural protein from striated muscle. II. Action on actin. , 1965, Journal of biochemistry.

[23]  T. Volk,et al.  A role for integrin in the formation of sarcomeric cytoarchitecture , 1990, Cell.

[24]  K. Wang,et al.  Nebulin as a length regulator of thin filaments of vertebrate skeletal muscles: correlation of thin filament length, nebulin size, and epitope profile , 1991, The Journal of cell biology.

[25]  R. Waterston,et al.  Cloning, sequencing, and mapping of an α-actinin gene from the nematode Caenorhabditis elegans , 1991 .

[26]  J. Files,et al.  Actin gene family of Caenorhabditis elegans. , 1983, Journal of molecular biology.

[27]  Seungho Wang,et al.  Skeletal muscle myofibrillogenesis as revealed with a monoclonal antibody to titin in combination with detection of the α- and γ-isoforms of actin , 1989 .

[28]  J. Murray,et al.  The vinculin/sarcomeric-alpha-actinin/alpha-actin nexus in cultured cardiac myocytes , 1992, The Journal of cell biology.

[29]  P. Maher,et al.  Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. II. Generation of alpha-actinin dots within titin spots at the time of the first myofibril formation , 1987, The Journal of cell biology.

[30]  R. H. Warren MICROTUBULAR ORGANIZATION IN ELONGATING MYOGENIC CELLS , 1974, The Journal of cell biology.

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

[32]  S. Ebashi,et al.  Alpha-actinin, a new structural protein from striated muscle. I. Preparation and action on actomyosinàtp interaction. , 1965, Journal of biochemistry.

[33]  E. Fyrberg,et al.  Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. , 1989, Genes & development.

[34]  Kuan Wang,et al.  Nebulin as a giant actin‐binding template protein in skeletal muscle sarcomere Interaction of actin and cloned human nebulin fragments , 1991, FEBS letters.

[35]  K. Mark,et al.  Antagonistic effects of laminin and fibronectin on the expression of the myogenic phenotype , 1989 .

[36]  K. Wang,et al.  Cloning, expression, and protein interaction of human nebulin fragments composed of varying numbers of sequence modules. , 1991, The Journal of biological chemistry.

[37]  R. Lehmann,et al.  The function of PS integrins during Drosophila embryogenesis , 1989, Cell.

[38]  K. Weber,et al.  The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line , 1988, The Journal of cell biology.

[39]  R. K. Herman,et al.  Duplications in Caenorhabditis elegans. , 1979, Genetics.

[40]  S. Strome Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans , 1986, The Journal of cell biology.

[41]  Jonathan A. Cooper,et al.  Effects of CapZ, an actin capping protein of muscle, on the polymerization of actin. , 1989, Biochemistry.

[42]  S. Haskill,et al.  Signal transduction from the extracellular matrix , 1993, The Journal of cell biology.

[43]  T. Gibson,et al.  Evidence that nebulin is a protein‐ruler in muscle thin filaments , 1991, FEBS letters.

[44]  R. Waterston,et al.  Vinculin is essential for muscle function in the nematode , 1991, The Journal of cell biology.

[45]  D. Moerman,et al.  Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. , 1993, Genes & development.

[46]  R. Waterston,et al.  Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization , 1985, The Journal of cell biology.

[47]  R. Hall,et al.  Relationship of Muscle Apolipoprotein E Expression with Markers of Cellular Stress, Metabolism, and Blood Biomarkers in Cognitively Healthy and Impaired Older Adults , 2023, Journal of Alzheimer's disease : JAD.

[48]  H. F. Epstein,et al.  Muscle differentiation in normal and cleavage-arrested mutant embryos of Caenorhabditis elegans , 1982, Cell.

[49]  E. Raff,et al.  The beta 3-tubulin gene of Drosophila melanogaster is essential for viability and fertility. , 1990, Genetics.

[50]  J. Casella,et al.  Purification and initial characterization of a protein from skeletal muscle that caps the barbed ends of actin filaments. , 1986, The Journal of biological chemistry.

[51]  T. Wright,et al.  A histological and ultrastructural analysis of developmental defects produced by the mutation, lethal(1)myospheroid, in Drosophila melanogaster. , 1981, Developmental biology.

[52]  T. Bogaert,et al.  Positioning and maintenance of embryonic body wall muscle attachments in C. elegans requires the mup-1 gene. , 1991, Development.

[53]  Jonathan A. Cooper,et al.  Localization of CapZ during myofibrillogenesis in cultured chicken muscle. , 1993, Cell motility and the cytoskeleton.

[54]  J. Lessard Two monoclonal antibodies to actin: one muscle selective and one generally reactive. , 1988, Cell motility and the cytoskeleton.

[55]  C. Turner,et al.  Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. , 1988, Annual review of cell biology.

[56]  T. Gibson,et al.  A regular pattern of two types of 100-residue motif in the sequence of titin , 1990, Nature.

[57]  R. Cripps,et al.  Molecular genetic analysis of muscle development, structure, and function in Drosophila. , 1993, International review of cytology.

[58]  E. Raff,et al.  A variant beta-tubulin isoform of Drosophila melanogaster (beta 3) is expressed primarily in tissues of mesodermal origin in embryos and pupae, and is utilized in populations of transient microtubules. , 1989, Developmental biology.

[59]  R. Waterston,et al.  Muscle cell attachment in Caenorhabditis elegans , 1991, The Journal of cell biology.

[60]  A. C. Crossley,et al.  morphology and development of the Drosophila muscular system , 1978 .

[61]  H. Holtzer,et al.  AN ANALYSIS OF MYOGENESIS BY THE USE OF FLUORESCENT ANTIMYOSIN , 1957, The Journal of biophysical and biochemical cytology.

[62]  H. F. Epstein,et al.  Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages , 1993, Journal of Cell Biology.

[63]  R. Waterston,et al.  Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations , 1994, The Journal of cell biology.

[64]  J. Trinick,et al.  Does titin regulate the length of muscle thick filaments? , 1989, Journal of molecular biology.

[65]  K. von der Mark,et al.  Antagonistic effects of laminin and fibronectin on the expression of the myogenic phenotype. , 1989, Differentiation; research in biological diversity.

[66]  David M. Miller,et al.  Differential localization of two myosins within nematode thick filaments , 1983, Cell.

[67]  J. Karn,et al.  Immunological identification of the genes encoding the four myosin heavy chain isoforms of Caenorhabditis elegans. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[68]  K. Weber,et al.  Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly , 1989, The Journal of cell biology.

[69]  A. Eisen,et al.  Integrin α2β1 (VLA-2) mediates reorganization and contraction of collagen matrices by human cells , 1991, Cell.

[70]  R. Robson,et al.  Properties of smooth muscle vinculin. , 1984, The Journal of biological chemistry.

[71]  R. Waterston,et al.  The basal component of the nematode dense-body is vinculin. , 1989, The Journal of biological chemistry.

[72]  P. Cheng,et al.  The development of myofibrils in cultured muscle cells: a whole-mount and thin-section electron microscopic study. , 1981, Developmental biology.

[73]  M. Reedy,et al.  Molecular genetics of Drosophila alpha-actinin: mutant alleles disrupt Z disc integrity and muscle insertions , 1990, The Journal of cell biology.

[74]  R. Devlin,et al.  Coordinate regulation of contractile protein synthesis during myoblast differentiation , 1978, Cell.

[75]  A. Horwitz,et al.  Myoblast migration specifically inhibited in the chick embryo by grafted CSAT hybridoma cells secreting an anti-integrin antibody. , 1988, Development.

[76]  G. Piperno,et al.  Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms , 1985, The Journal of cell biology.

[77]  P. Antin,et al.  Role of stress fiber-like structures in assembling nascent myofibrils in myosheets recovering from exposure to ethyl methanesulfonate , 1986, The Journal of cell biology.

[78]  R. Waterston Molecular genetic approaches to the study of motility in Caenorhabditis elegans. , 1989, Cell motility and the cytoskeleton.