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Role of intestinal mucus in crystal biogenesis: an electron-microscopical, diffraction and X-ray microanalytical study

Cell and Tissue Research volume 255, pages 575–583 (1989)Cite this article

Summary

In the posterior intestine of the sea-water eel, mucus plays an important role in biocrystallization of calcium ions. By means of transmission and scanning electron microscopy associated with X-ray microanalysis and X-ray diffraction it has been possible to determine the role of mucous fibers as nucleation sites. Biocrystallization occurs in 2 steps: (1) Calcification of mucus. As soon as mucus is excreted in the intestinal lumen, it is loaded with calcium, as shown by lanthanum affinity and X-ray microanalysis on freeze-dried tissues. (2) Genesis of crystals. Needleshaped crystallites build up in coalescent spherites in the intestinal lumen near the microvilli. Genesis occurs as follows: (a) crystallite mineralization by nucleation in an organic matrix composed of glycoproteinaceous mucous fibers, followed by the appearance of spherites; (b) coalescence in spherites and association of spherites in rhombohedra; (c) extrusion of organic material during the final step of crystallization.

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References

  • Allen A, Pain RH, Robsen TR (1976) Model for the structure of the gastric mucous gel. Nature 264:88–89

    Google Scholar 

  • American Society for Testing Materials (ASTM): X-ray powder diffraction file card n∘ 24–27 (1965) and 25–127 (1969)

  • Addadi L, Weiner S (1985) Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci USA 82:4110–4114

    Google Scholar 

  • Addadi L, Moradian J, Shay E, Maroudas NG, Weiner S (1987) A chemical model for the cooperation of sulfates and carboxylates in calcite crystal nucleation: relevance to biomineralization. Proc Natl Acad Sci USA 84:2732–2736

    Google Scholar 

  • Arnaud JP, Humbert W, Eloy R, Ollier JC, Bruant P, Adloff M (1981) Lithiase pancréatique. Apport de la microscopie électronique à balayage, de la cristallographie et de la spectrographie aux rayons X. Med Chir Dig 10:613–616

    Google Scholar 

  • Arnott HJ (1982) Three systems of biomineralization in plants withcomments on the associated matrix. In: Nancollas GH (ed) Biological mineralization and demineralization. Dahlem Konferenzen. Springer, Berlin Heidelberg New York, pp 199–218

    Google Scholar 

  • Boquet E, Boronat A, Ramos-Cormenzana A (1973) Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246:527–528

    Google Scholar 

  • Crowther RS, Marriott C (1984) Counter-ion binding to mucus glycoproteins. J Pharm Pharmacol 36:21–26

    Google Scholar 

  • Doggenweiler CF, Frenk S (1965) Staining properties of lanthanum on cell membranes. Proc Natl Acad Sci USA 53:423–430

    Google Scholar 

  • Dykstra M, Hackett RL (1979) Ultrastructural events in early calcium oxalate crystal formation in rats. Kidney Int 15:640–644

    Google Scholar 

  • Eanes ED, Posner AS (1965) Kinetics and mechanisms of conversion of non crystalline calcium phosphate to crystalline hydroxyapatite. Trans NY Acad Sci 28:233–241

    Google Scholar 

  • Eanes ED, Termine JD, Nylen M (1973) An electron microscope study of the formation of amorphous calcium phosphate and its transformation to crystalline apatite. Calc Tissue Res 12:143–158

    Google Scholar 

  • Epivatianos A, Harrison JD, Garrett JR, Davies KJ, Senkus R (1986) Ultrastructural and histochernical observations on intracellular and luminal microcalculi in the feline sublingual salivary gland. J Oral Pathol 15:513–517

    Google Scholar 

  • Fleisch H (1982) Mechanisms of normal mineralization in bone and cartilage. In: Nancollas GH (ed) Biological mineralization and demineralization. Dahlen Konferenzen. Springer, Berlin Heidelberg New York, pp 233–241

    Google Scholar 

  • Glimcher MJ (1981) On the form and function of bone: from molecules to organs. Wolffs law revisited. In: Veis A (ed) The chemistry and biology of mineralized connective tissues. Elsevier, New York, pp 617–673

    Google Scholar 

  • Hoffstein S, Gennard DE, Fox AC, Hirsch J, Streuli F, Weissmann G (1975) Colloidal lanthanum as a marker for impaired plasma permeability in ischemic dog myocardium. Am J Pathol 79:207–214

    Google Scholar 

  • Humbert W (1978) Intracellular and intramitochondrial binding of lanthanum in dark degenerating midgut cells of a collembolan (Insect). Histochemistry 59:117–128

    Google Scholar 

  • Humbert W (1979) Les organes excréteurs des Collemboles: étude ultrastructurale, cytochimique, spectrographique et approche écophysiologique. Thèse d'Etat n∘1187, Strasbourg

  • Humbert W, Arnaud JP, Eloy R, Adloff M (1980) Lanthanum penetration into cancerous colonic cells: a microanalytical study. In: Bailey GW (ed) 38th Ann Proc: Electron microscopy, Soc Am California, pp 732–733

  • Humbert W, Kirsch R, Simonneaux V (1986) Is mucus involvedin biocrystallization? Study of the intestinal mucus of the sea water eel Anguilla anguilla L. Cell Tissue Res 245:599–604

    Google Scholar 

  • Jehl B, Bauer R, Dörge A, Rick R (1981) The use of propane isopentane mixtures for rapid freezing of biological specimens. J Microsc 123:307–309

    Google Scholar 

  • Johannessen JV, Sobrinho-Simoes M (1980) The origin and significance of thyroid psammoma bodies. Lab Invest 43:287–296

    Google Scholar 

  • Kirsch R, Humbert W, Rodeau JL (1984) Control of the blood osmolarity in fishes with references to the functional anatomy of the gut. In: Péqueux A, Gilles R, Bolis L (eds) Osmoregulation in Estuarine and Marine Animals. Springer, Berlin Heidelberg New York, pp 67–92

    Google Scholar 

  • Kirsch R, Humbert W, Simonneaux V (1985) The gut as an osmoregulatory organ: comparative aspects and special references to fishes: In: Gilles R, Gilles-Baillien M (eds) Transport processes, iono- and osmoregulation. Springer, Berlin Heidelberg New York, pp 265–277

    Google Scholar 

  • Kirsch R, Barra JA, Humbert W, Simmonneaux V (1987) Mucus and epithelial exchanges. In: Comparative Physiology of environmental adaptations, vol 1, 8th ESCPB Conference Strasbourg 1986, Karger, Basel, pp 158–168

    Google Scholar 

  • Lee SP, La Mont JT, Carey MC (1981) Role of gallbladder mucus hypersecretion in the evolution of cholesterol gallstones. J Clin Invest 67:1712–1723

    Google Scholar 

  • Levy PE, Smith BF, La Mont JT (1984) Human gall-bladder mucin accelerates nucleation of cholesterol in artificial bile. Gastroenterology 87:270–275

    Google Scholar 

  • Loewenstam HA (1981) Minerals formed by organisms. Science 211:1126–1131

    Google Scholar 

  • Loewenstam HA, Weiner S (1983) Mineralization by organisms and the evolution of biomineralization. In: Westbroek P, De Jong EW (eds) Biomineralization and biological metal accumulation, Dordrecht, Reidel, pp 191–203

    Google Scholar 

  • Lucas J, Prévôt L (1984) Synthèse de l'apatite par voie bactérienne à partir de matière organique phosphatée et de divers carbonates de calcium dans des eaux douce et marine naturelles. Chem Geol 42:101–118

    Google Scholar 

  • Maki T, Matsushiro T, Suzuki N, Nakamura N (1971) Role of sulfate glycoproteins in gallstone formation. Surg Gyn Obstet 132:846–854

    Google Scholar 

  • Matthews JL, Arnott HJ, Brown WE, Dosch W, Hascall VC, Hautmann R, Krampitz GP, Münzenberg KJ, Pritzker KPH, Prockop DJ, Schenk RK, Watabe N, Young RA (1982) Structure, properties and function of mineralized tissue components. In: Nancollas GH (ed) Biological mineralization and demineralization. Dahlem Konferenzen, Springer, Berlin Heidelberg New York, pp 327–348

    Google Scholar 

  • Meister MF, Humbert W, Kirsch R, Vivien-Roels B (1983) Structure and ultrastructure of the oesophagus in sea-water and fresh-water teleosts (Pisces). Zoomorphology 102:33–51

    Google Scholar 

  • Nancollas GH (1979) The growth of crystals in solution. Adv Colloid Interface Sci 10:215–252

    Google Scholar 

  • Parmelee JT, Renfro JL (1983) Esophageal desalination of seawater in flounder: role of active sodium transport. Am J Physiol 245:R888-R893

    Google Scholar 

  • Ross MD, Pote KG (1984) Some properties of otoconia. Philos Trans R Soc Lond [Biol] 304:445–452

    Google Scholar 

  • Scott JE (1968) Ion binding in solutions containing acid mucopolysaccharides. In: Quintarelli G (ed) Chemical physiology of mucopolysaccharides. Little, Brown and Company, Boston, pp 171–185

    Google Scholar 

  • Simkiss K (1976) Intracellular and extracellular routes in biomineralization. Symp Soc Exp Biol, pp 423–444

  • Simonneaux V, Barra JA, Humbert W, Kirsch R (1987a) Mucus role in ion absorption by the oesophagus of the sea-water eel (Anguilla anguilla L): electrophysiological, structural and cytochemical investigations. J Comp Physiol B 157:187–199

    Google Scholar 

  • Simonneaux V, Humbert W, Kirsch R (1987b) Mucus and intestinal ion exchanges in the sea water adapted eel, Anguilla anguilla L. J Comp Physiol B 157:295–306

    Google Scholar 

  • Voegel JC, Frank RM (1974) Diffraction electronique monocristalline de l'émail humain sain et carié. J Biol Buc 2:153–160

    Google Scholar 

  • Weiner S, Traub W (1984) Macromolecules in mollusc shells and their functions in biomineralization. Philos Trans R Soc Lond [Biol] 304:409–558

    Google Scholar 

  • Weiner S, Traub W, Loewenstam H (1983) Organic matrix in calcified exoskeletons. In: Westbroek P, De Jong EW (eds) Biomineralization and biological metal accumulation, Reidel, Dordrecht, Holland, pp 205–224

    Google Scholar 

  • Westbroek P, De Jong EW, Van der Wal P, Borman AH, De Vrind JPM, Kok D, De Bruijn WC, Parker SB (1984) Mechanisms of calcification in the marine alga Emiliania huxleyi. Philos Trans R Soc Lond [Biol] 304:435–444

    Google Scholar 

  • Wijsma TCM (1975) pH fluctuations in Mytilus edulis L. in relation to shell movements under aerobic and anaerobic conditions. In: Barnes H (ed) The Biochemistry, Physiology and Behavior of Marine Organisms in relation to their ecology, Aberdeen University of Aberdeen Press, pp 139–149

  • Williams RJP (1984) An introduction to biominerals and the role of organic molecules in their formation. Philos Trans R Soc Lond [Biol] 304:411–424

    Google Scholar 

  • Womack NA (1971) The development of gallstones. Surg Gyn Obst 133:937–945

    Google Scholar 

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Affiliations

  1. Université Louis Pasteur, Laboratoire de Zoologie, CNRS LIRA 226, Strasbourg, France

    W. Humbert, R. Kirsch & V. Simonneaux

  2. Centre de Recherches Odontologiques, INSERM U157, Strasbourg, France

    J. C. Voegel

Authors
  1. W. Humbert
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  2. J. C. Voegel
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  3. R. Kirsch
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  4. V. Simonneaux
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Humbert, W., Voegel, J.C., Kirsch, R. et al. Role of intestinal mucus in crystal biogenesis: an electron-microscopical, diffraction and X-ray microanalytical study. Cell Tissue Res. 255, 575–583 (1989). https://doi.org/10.1007/BF00218793

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  • DOI: https://doi.org/10.1007/BF00218793

Key words

  • Intestinal mucus
  • Biocrystallization
  • X-ray microanalysis
  • Electron diffraction
  • X-ray diffraction
  • Eel (Anguilla anguilla)