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Ultrastructural localization of cholinesterase uring chondrogenesis and myogenesis in the chick limb bud

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Summary

Cholinesterase (ChE) is transiently expressed in undifferentiated embryonic cells. In the chick limb bud ChE-activity was found in the apical ectodermal ridge and in the subridge mesenchyme. The reaction was localized in the perinuclear cisterna, in an extensive network of narrow profiles of endoplasmic reticulum (ER), and in the Golgi complex

The chondroblasts emerging from the subridge mesenenyme, also showed strong ChE-activity. During differentiation the enzyme first disappeared from the Golgi zone. Then, the narrow ChE-positive ER was successively replaced by ChE-negative extended rough ER characteristic for the differentiated chondrocyte.

The myoblasts showed weak ChE-activity with the same ultrastructural localization as in other mesenchymal cells. After fusion the myotubes exhibited strong ChE-activity in the perinuclear cisterna and the developing sarcoplasmic reticulum. In later stages of myogenesis the myoblasts were closely attached to the myotubes and had lost their ChE-activity.

During mitosis of ChE-positive cells, ChE-activity was retained in fragments of perinuclear cisterna and ER. In ChE-active mesenchymal cells and chondroblasts we observed specialized contact zones between ER and plasma membrane. ChE-active cisternae of ER run parallel to the plasma membrane with a gap of approximately 10–15 nm. We discuss a possible function of a cholinergic system during morphogenesis.

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References

  • Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186

    Google Scholar 

  • Cochard P, Coltey P (1983) Cholinergic traits of the neural crest: acetylcholinesterase in crest cells of the chick embryo. Dev Biol 98:221–238

    Google Scholar 

  • Dalton AJ (1955) A chrome-osmium fixative for electron microscopy. Anat Rec 121:181

    Google Scholar 

  • Drews U (1965) Über das Verhalten der Esterasen insbesondere der Cholinesterase-Aktivität in der Nebennierenregion der Ratte während der Fetalzeit. Histochemie 4:514–530

    Google Scholar 

  • Drews U (1975) Cholinesterase in embryonic development. Prog Histochem Cytochem vol 7/3, Gustav Fischer, Stuttgart

    Google Scholar 

  • Drews U, Drews U (1972) Cholinesterase in der Extremitätenentwicklung des Hühnchens: I. Phasen der Cholinesterase-Aktivität in der jungen Knospe und bei der Abgrenzung von Knorpel-und Muskelanlagen. Wilhelm Roux' Arch Entwicklungsmech Org 169:70–86

    Google Scholar 

  • Drews U, Drews U (1973) Cholinesterase in der Extremitätenentwicklung des Hühnchens: II. Fermentaktivität und Bewegungsverhalten der präsumptiven Knorpelzellen in vitro. Wilhelm Roux' Arch Entwicklungsmech Org 173:208–227

    Google Scholar 

  • Ede DA, Wilby OK (1981) Golgi orientation and cell behaviour in the developing pattern of chondrogenic condensations in chick limb bud mesenchyme. Histochem J 13:615–630

    Google Scholar 

  • Ede DA, Flint OP, Wilby OK, Colquhoun P (1977) The development of precartilage condensations in limb bud mesenchyme in vivo and in vitro. In: Ede DA, Hinchliffe JR, Balls M (eds) Vertebrate limb and somite morphogenesis, pp 161–179, Cambridge University Press

  • Fluck RA (1982) Localization of acetylcholinesterase activity in young embryos of the medaka oryzias latipes, a teleost. Comp Biochem Physiol 72C:59–64

    Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–67

    Google Scholar 

  • Hilfer SR, Searls RL, Fonte VG (1973) An ultrastructural study of early myogenesis in the chick wing bud. Dev Biol 30:374–391

    Google Scholar 

  • Jacob M, Christ B, Jacob HJ (1978) On the migration of myogenic stem cells into the prospective wing region in chick embryos: A scanning and transmission electron microscope study. Anat Embryol 153:179–193

    Google Scholar 

  • Jurand A (1965) Ultrastructural aspects of early development of the forelimb buds in the chick and mouse. Proc Roy Soc Ser B 162:387–405

    Google Scholar 

  • Karnovsky MJ (1964) The localization of cholinesterase activity in rat cardiac muscle by electron microscopy. J Cell Biol 23:217–232

    Google Scholar 

  • Karnovsky MJ, Roots L (1964) A “Direct-coloring” thiocholine method for cholinesterase. J Histochem Cytochem 12:219–221

    Google Scholar 

  • Kosher RA, Savage MP, Chan SC (1979) In vitro studies on the morphogenesis and differentiation of the mesoderm subjacent to the apical ectodermal ridge of the chick limb bud. J Embryol Exp Morphol 50:75–97

    Google Scholar 

  • Kreutzberg GW, Toth L, Kaiya H (1975) Acetylcholinesterase as a marker for dendritic transport and dendritic secretion. Adv Neurol 12:269–281

    Google Scholar 

  • Layer GL (1983) Comparative localization of acetylcholinesterase and pseudocholinesterase during morphogenesis of the chicken brain. Proc Natl Acad Sci USA 80:6413–6417

    Google Scholar 

  • Lewis PR, Shute CCD (1969) An electron microscopic study of cholinesterase distribution in the rat adrenal medulla. J Micros 89:181–193

    Google Scholar 

  • Majcen Ž, Brzin M (1979) Cholinesterase and choline acetyltransferase in the longitudinal muscle of the guinea pig ileum. Histochemistry 63:295–302

    Google Scholar 

  • Miki A, Mizoguti H (1982a) Proliferating ability, morphological development and acetylcholinesterase activity of the neural tube cells in early chick embryos. An electron microscopic study. Histochemistry 76:303–314

    Google Scholar 

  • Miki A, Mizoguti H (1982b) Acetylcholinesterase activity in the myotome of the early chick embryo. Cell Tissue Res 227:23–40

    Google Scholar 

  • Miki A, Fujimoto E, Mizoguti H (1983) Acetylcholinesterase activity in neural crest cells of the early chick embryo. Histochemistry 78:81–93

    Google Scholar 

  • Milaire J, Duchesnes C (1979) Etudes de quelques propriétés structurales et histochimiques du mésoblaste marginal des bourgeons de membranes de l'embryon de poulet (stades 20 à 26). Arch Anat Micr Morphol Exp 68:169–193

    Google Scholar 

  • Mumenthaler M, Engel WK (1961) Cytological localization of cholinesterase in developing chick embryo skeletal muscle. Acta Anat 47:274–299

    Google Scholar 

  • Newman SA, Pautou MP, Kieny M (1981) The distal boundary of myogenic primordia in chimeric avian limb buds and its relation to an accessible population of cartilage progenitor cells. Dev Biol 84:440–448

    Google Scholar 

  • Oettling G, Schmidt H, Drews U (1985) The muscarinic receptor of chick embryo cells: correlation between ligand binding and calcium mobilization. J Cell Biol 100:1073–1082

    Google Scholar 

  • Penner PL, Brick I (1984) Acetylcholinesterase and poly-ingression in the epiblast of the primitive streak chick embryo. Roux's Arch Dev Biol 193:234–241

    Google Scholar 

  • Reich A, Drews U (1983) Choline acetyltransferase in the chick limb bud. Histochemistry 78:383–389

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Schmidt H (1981) Muscarinic acetylcholine receptor in chick limb bud during morphogenesis. Histochemistry 71:89–98

    Google Scholar 

  • Schmidt H, Oettling G, Kaufenstein T, Hartung G, Drews U (1984) Intracellular calcium mobilization on stimulation of the muscarinic cholinergic receptor in chick limb bud cells. Roux's Arch Dev Biol 194:44–49

    Google Scholar 

  • Schröder C (1980) Characterization of embryonic cholinesterase in chick limb bud by colorimetry and disk electrophoresis. Histochemistry 69:243–253

    Google Scholar 

  • Searls RL, Hilfer SR, Mirow SM (1972) An ultrastructural study of early chondrogenesis in the chick wing bud. Dev Biol 28:123–137

    Google Scholar 

  • Tennyson VM, Brzin M, Slotwiner P (1971) The appearance of acetylcholinesterase in the myotome of the embryonic rabbit: An electron microscopic cytochemical and biochemical study. J Cell Biol 51:703–721

    Google Scholar 

  • Tennyson VM, Brzin M, Kremzner LT (1973) Acetylcholine-esterase activity in the myotome and muscle satellite cell of the fetal rabbit: An electron microscopic-cytochemical and biochemical study. J Histochem Cytochem 21:634–652

    Google Scholar 

  • Venable JH, Coggeshall R (1965) A simplified lead citrate for use in electron microscopy. J Cell Biol 25:407–408

    Google Scholar 

  • Wachtler F, Christ B, Jacob HJ (1981) On the determination of mesodermal tissues in the avian embryonic wing bud. Anat Embryol 161:283–289

    Google Scholar 

  • Zimmermann B, Scharlach E, Kaatz R (1982) Cell contact and surface coat alterations of limb bud mesenchymal cells during differentiation. J Embryol Exp Morphol 72:1–18

    Google Scholar 

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  1. Anatomisches Institut, Österbergstr. 4, D-7400, Tübingen 1, Federal Republic of Germany

    Pramote Vanittanakom &  Ulrich Drews

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  1. Pramote Vanittanakom
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  2. Ulrich Drews
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Vanittanakom, P., Drews, U. Ultrastructural localization of cholinesterase uring chondrogenesis and myogenesis in the chick limb bud. Anat Embryol 172, 183–194 (1985). https://doi.org/10.1007/BF00319601

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