Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth.

The fine structure of tendon fibroblasts in developing limbs of chick and mouse embryos have been examined to define the cellular features of collagen fibrillogenesis in vivo . Two structural features of the fibroblast which may relate to fibril assembly have been observed: intracellular aggregates resembling SLS (segment-long-spacing)-like aggregates of monomeric and dimeric lengths and deep recesses of the cell surface containing striated fibrils. A model is proposed which suggests that assembly of a collagen fibril in vivo begins by formation of subassemblies inside the cell which then are excreted by exocytosis and added to a unique region at the fibril end. This end is closely associated with the cell surface in a manner which allows for cellular regulation of some parameters of fibril morphology.

[1]  M. Karnovsky,et al.  A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron-microscopy , 1965 .

[2]  Kuy Pérez-Tamayo,et al.  THE OCCURRENCE AND SIGNIFICANCE OF SLS CRYSTALLITES IN VIVO , 1972 .

[3]  Welsh Ra,et al.  Intracellular collagen fibers. In human mesenchymal tumors and inflammatory states. , 1967 .

[4]  R. Bruns,et al.  Procollagen segment-long-spacing crystallites: their role in collagen fibrillogenesis. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[5]  T. Greenlee,et al.  A fine structural study of the development of the chick flexor digital tendon: a model for synovial sheathed tendon healing. , 1975, The American journal of anatomy.

[6]  L. Lukens.  Time of occurrence of disulfide linking between procollagen chains. , 1976, The Journal of biological chemistry.

[7]  L. Kohn,et al.  Calf tendon procollagen peptidase: its purification and endopeptidase mode of action. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Bruns,et al.  High‐resolution analysis of the modified quarter‐stagger model of the collagen fibril , 1974, Biopolymers.

[9]  N. Blackett,et al.  A simplified method of "hypothetical grain" analysis of electron microscope autoradiographs. , 1977, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[10]  P. Bornstein,et al.  Procollagen: Conversion of the Precursor to Collagen by a Neutral Protease , 1972, Science.

[11]  C. P. Leblond,et al.  SYNTHESIS, MIGRATION, AND RELEASE OF PRECURSOR COLLAGEN BY ODONTOBLASTS AS VISUALIZED BY RADIOAUTOGRAPHY AFTER [3H]PROLINE ADMINISTRATION , 1974, The Journal of cell biology.

[12]  A. Veis,et al.  Intracellular location of triple helix formation of collagen. Enzyme probe studies. , 1976, The Journal of biological chemistry.

[13]  J. Gross,et al.  Morphologic studies of connective tissue resorption in the tail fin of metamorphosing bullfrog tadpole. , 1965, Developmental biology.

[14]  P. Parakkal.  INVOLVEMENT OF MACROPHAGES IN COLLAGEN RESORPTION , 1969, The Journal of cell biology.

[15]  J. Gross.  THE BEHAVIOR OF COLLAGEN UNITS AS A MODEL IN MORPHOGENESIS , 1956, The Journal of biophysical and biochemical cytology.

[16]  R. Dyer,et al.  Intracellular collagen in the nonpregnant and IUD‐containing rat uterus , 1977, The Anatomical record.

[17]  Ferrans Vj,et al.  Intracellular collagen fibrils in cardiac valves of patients with the Hurler syndrome. , 1976 .

[18]  R. Frank.  Etude autoradiographique de la dentinogenese en microscopie electronique a l'aide de la proline tritiee chez le chat , 1970 .

[19]  A. Veis,et al.  A Limiting Microfibril Model for the Three-dimensional Arrangement within Collagen Fibres , 1967, Nature.

[20]  F. Silver,et al.  Type I Collagen Fibrillogenesis: Initiation via Reversible Linear and Lateral Growth Steps , 1979, Biopolymers.

[21]  M. Salpeter,et al.  Resolution of electron microscope autoradiography. IV. Application to analysis of autoradiographs , 1978, The Journal of cell biology.

[22]  T. Greenlee,et al.  The development of human digital tendons. , 1975, Journal of anatomy.

[23]  G. C. Wood,et al.  The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. , 1960, The Biochemical journal.

[24]  R. Trelstad,et al.  Collagen fibrillogenesis: intermediate aggregates and suprafibrillar order. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[25]  K. Piez,et al.  Collagen fibril formation. Optimal in vitro conditions and preliminary kinetic results. , 1978, The Journal of biological chemistry.

[26]  B. Goldberg.  Electron microscopic studies of procollagen from cultured human fibroblasts , 1974 .

[27]  J. Uitto,et al.  Purification and partial characterization of the type II procollagen synthesized by embryonic cartilage cells. , 1977, Archives of biochemistry and biophysics.

[28]  J. Gross,et al.  The heat precipitation of collagen from neutral salt solutions: some rate-regulating factors. , 1958, The Journal of biological chemistry.

[29]  K. Porter,et al.  Collagen Formation by Fibroblasts of the Chick Embryo Dermis , 1959, The Journal of biophysical and biochemical cytology.

[30]  G. Palade,et al.  Intracellular aspects of the process of protein synthesis. , 1975, Science.

[31]  T. Nakao.  Fine structure of the myotendinous junction and “terminal coupling” in the skeletal muscle of the lamprey, Lampetra japonica , 1975, The Anatomical record.

[32]  D. Jackson,et al.  The sub-cellular location of inter-chain disulfide bond formation during procollagen biosynthesis by embryonic chick tendon cells. , 1973, Biochemical and biophysical research communications.

[33]  A. R. Cate.  Morphological studies of fibrocytes in connective tissue undergoing rapid remodelling. , 1972 .

[34]  M. Stearns.  Studies on the development of connective tissue in transparent chambers in the rabbit's ear. II† , 1940 .

[35]  M. Taubman,et al.  Procollagen peptidase: Its mode of action on the native substrate , 1975, Cell.

[36]  R. Ross,et al.  EFFECTS OF ANTIMICROTUBULAR AGENTS ON THE SECRETION OF COLLAGEN , 1974, The Journal of cell biology.

[37]  B. Toole,et al.  EPITHELIAL COLLAGENS AND GLYCOSAMINOGLYCANS IN THE EMBRYONIC CORNEA , 1974, The Journal of cell biology.

[38]  J. W. SMITH,et al.  Molecular Pattern in Native Collagen , 1968, Nature.

[39]  R A Berg,et al.  The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen. , 1973, Biochemical and biophysical research communications.

[40]  J. Rosenbloom,et al.  Hydroxyproline content determines the denaturation temperature of chick tendon collagen. , 1973, Archives of biochemistry and biophysics.

[41]  S Glagov,et al.  Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. , 2003, Science.

[42]  M. Keech.  The formation of fibrils from collagen solutions. IV. Effect of mucopolysaccharides and nucleic acids: an electron microscope study. , 1961 .

[43]  D. Pease,et al.  The tridimensional structure of native collagenous fibrils, their proteinaceous filaments. , 1971, Journal of ultrastructure research.

[44]  B. Olsen,et al.  Further characterization of embryonic tendon fibroblasts and the use of immunoferritin techniques to study collagen biosynthesis , 1975, The Journal of cell biology.

[45]  N. Morris,et al.  Procollagen assembly and secretion in embryonic chick bone. , 1975, The Journal of biological chemistry.

[46]  R. Trelstad.  VACUOLES IN THE EMBRYONIC CHICK CORNEAL EPITHELIUM, AN EPITHELIUM WHICH PRODUCES COLLAGEN , 1971, The Journal of cell biology.

[47]  M. Weinstock.  Centrosymmetrical cross-banded structures in the matrix of rat incisor predentin and dentin. , 1977, Journal of ultrastructure research.

[48]  J. Weidemann,et al.  A morphological and biochemical examination of the hydrothermal denaturation of collagen. , 1978, Meat science.

[49]  D H ELLIOTT,et al.  STRUCTURE AND FUNCTION OF MAMMALIAN TENDON , 1965, Biological reviews of the Cambridge Philosophical Society.

[50]  D. Maccallum,et al.  Collagen structure: evidence for a helical organization of the collagen fibril. , 1977, Journal of ultrastructure research.

[51]  E. Hay,et al.  SECRETION OF COLLAGEN BY CORNEAL EPITHELIUM , 1973, The Journal of cell biology.

[52]  R. Trelstad,et al.  A simplified technique for electron microscope autoradiography. , 1976, Stain technology.

[53]  B. Olsen,et al.  Location of procollagen in chick corneal and tendon fibroblasts with ferritin-conjugated antibodies , 1975, The Journal of cell biology.