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Evolution of mesenchymal cells in fetal rat lung

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Summary

The evolution of connective tissue cells in the developing fetal rat lung is studied under the electron microscope from the 15th until the 21st day of gestation and is compared to the evolution of epithelial cells. Three successive types of stem cells (“mesocytoblasts”) are present during the first stages of lung development studied (15 to 18 days of gestation). These stem cells appear to be able to differentiate into fibroblasts or into smooth muscle cells, according to their localization along the broncho-alveolar tubule. Myoblasts are situated near the bronchial epithelium, whereas fibroblasts occur under the alveolar epithelium. Epithelo-mesenchymal interactions are assumed to play a role in this differentiation process. Synthesis of both, collagen and elastic fibers and of cytoplasmic filaments by fibroblasts as well as by myoblasts reveal the multiple potentialities of the mesenchymal stem cell and suggest a common origin.

The early fibroblast is characterized by long cytoplasmic processes which contain numerous cytofilaments, and by the presence of collagen fibers in the vicinity of the cell. Later on, (20 days of gestation) the mature fibroblast of the lung mesenchyme shows areas of RER, glycogen and lipidic vacuoles in its cytoplasm. Cytofilaments are numerous within very long cytoplasmic processes and elastic and collagen fibers are very frequent beside the cytoplasmic membrane.

The earliest fibroblast differentiation occurs under the epithelium of primitive respiratory bronchioles, which indicate the limit between the bronchial and the alveolar territories. Later on, differentiating fibroblasts are found throughout the whole alveolar walls.

Connective tissue cells other than mesenchymal stem cells, fibroblasts or myoblasts are observed during lung development. Vacuolar cells, similar to Hofbauer cells, transiently appear on the 16th day of gestation. On the 20th and the 21st day macrophage-like cells are present in the septal space of the alveolar wall. The absence of intermediate stages of differentiation and parallel evolution of blood cells suggest that those connective tissue cells are differentiated elsewhere and have then migrated from blood into lung mesenchyme. No cell death has been observed in the developing lung.

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References

  • Balis, J. U., Conen, P. E.: The role of alveolar inclusion bodies in the developing lung. Lab. Invest. 13, 1215–1229 (1964)

    Google Scholar 

  • Borghese, E.: Explanation experiments on the influence of the connective tissue capsule on the development of the epithelial part of the submandibular gland of Mus musculus. J. Anat. (Lond.) 84, 303–318 (1950)

    Google Scholar 

  • Brooker, B. E., Goodwin, L. G., Guy, M. W.: Ciliated fibroblasts in rabbit ear chambers. J. Anat. (Lond.) 110, 363–365 (1971)

    Google Scholar 

  • Calvo, W., Haas, R. J.: Die Histogenese des Knochenmarks der Ratte. Nerval Versorgung, Knochenmarkstroma und ihre Beziehung zur Blutzellbildung. Z. Zellforsch. 95, 377–395 (1969)

    Google Scholar 

  • Campiche, M. A., Gautier, A., Hernandez, E. I., Reymond, A.: An electron microscope study of the fetal development of human lung. Pediatrics 32, 976–994 (1963)

    Google Scholar 

  • Campiche, M. A.: L'ultrastructure pulmonaire chez le fœtus et le nouveau-né. Thèse Faculté de Médecine, Université de Lausanne, Suisse (1963)

  • Collet, A. J., Des Biens, G.: Fine structure of myogenesis and elastogenesis in the developing rat lung. Anat. Rec. 178, 343–359 (1974)

    Google Scholar 

  • Conen, P. E., Balis, J. U.: Electron microscopy in study of lung development. In: The anatomy of the developing lung, ed. J. Emery, p. 18–48. Kingswood Survey, England: W. Heinemann, Med. Books Ltd 1969

    Google Scholar 

  • Cutler, L. S., Chaudhry, A. P.: Intercellular contacts at the epithelio-mesenchymal interface during the prenatal development of the rat submandibular gland. Develop. Biol. 33, 229–240 (1973)

    Google Scholar 

  • Dameron, F.: Influence de divers mésenchymes sur la différenciation de l'épithélium pulmonaire de l'embryon de Poulet en culture in vitro. C.R. Acad. Sci. (Paris). 252, 3879–3881 (1961a)

    Google Scholar 

  • Dameron, F.: L'influence de divers mésenchymes sur la différenciation de l'épithélium pulmonaire de l'embryon de Poulet en culture in vitro. J. Embryol. exp. Morph. 9, 628–633 (1961b)

    Google Scholar 

  • Dameron, F.: Etude expérimentale de l'organogénèse du poumon: nature et spécificité des interactions épithelo-mésenchymateuses. J. Embryol. exp. Morph. 20, 151–167 (1968)

    Google Scholar 

  • Dempsey, E. E.: The development of capillaries in the villi of early human placentas. Amer. J. Anat. 134, 221–238 (1972)

    Google Scholar 

  • Emery, J.: Connective tissue and lymphatics. In: The anatomy of the developing lung, ed J. Emery, p. 49–73. Kingswood, Survey, England: W. Heinemann, Med. Books Ltd. 1969

    Google Scholar 

  • Enders, A. C., King, B. F.: The cytology of Hofbauer cells. Anat. Rec. 167, 231–251 (1970)

    Google Scholar 

  • Fonte, V. G., Searls, R. L., Hilfer, S. R.: The relationship of cilia with cell division and differentiation. J. Cell Biol. 49, 226–229 (1971)

    Google Scholar 

  • Frasca, J. M., Parks, V. R.: A routine technique for double-staining ultrathin sections using uranyl and lead salts. J. Cell Biol. 25, 157–160 (1965)

    Google Scholar 

  • Godman, G. C., Porter, K. R.: Chondrogenesis studied with the electron microscope. J. biophys. biochem. Cytol. 8, 719–760 (1960)

    Google Scholar 

  • Goldberg, B., Green, H.: An analysis of collagen secretion by established mouse fibroblast lines. J. Cell Biol. 22, 227–258 (1964)

    Google Scholar 

  • Greenlee, T. K., Ross, R.: The development of the Rat flexor digital tendon, a fine structure study. J. Ultrastruct. Res. 18, 354–376 (1967)

    Google Scholar 

  • Grobstein, C.: Analysis of the early organization of the rudiment of the mouse submandibular gland. J. Morph. 93, 19–44 (1953)

    Google Scholar 

  • Hirsch, J. G., Fedorko, M. E.: Ultrastructure of human leukocytes after simultaneous fixation with glutaraldehyde and osmium tetroxide and “postfixation” in uranyl acetate. J. Cell Biol. 38, 615–627 (1968)

    Google Scholar 

  • Kapanci, Y., Assimacopoulos, A., Irlé, C., Zwaheln, A., Gabbiani, G.: “Contractile interstitial cells” in pulmonary alveolar septa: a possible regulation of ventilation/perfusion ratio? J. Cell Biol. 60, 375–392 (1974)

    Google Scholar 

  • Kelly, R. O.: An electron microscopic study of mesenchyme during development of interdigital spaces in man. Anat. Rec. 168, 43–54 (1970)

    Google Scholar 

  • Kikkawa, Y., Motoyama, E. K., Gluck, L.: Study of the lungs of fetal and newborn rabbits. Amer. J. Path. 52, 177–209 (1968)

    Google Scholar 

  • Kindred, J. E., Corey, E. L.: Studies on the blood of the fetal albino rat. Anat. Rec. 47, 213–227 (1930)

    Google Scholar 

  • Leeson, T. S., Leeson, C. R.: A light and electron microscope study of developing respiratory tissue in the rat. J. Anat. (Lond.) 98, 183–193 (1964)

    Google Scholar 

  • Loosli, C. G., Potter, E. L.: Pre-and postnatal development of the respiratory portion of the human lung. Amer. Rev. resp. Dis. 80 Part II (Supplt) 5–20 (1959)

    Google Scholar 

  • Marin, L., Dameron, F.: Evolution en greffe hétérochronique de l'ébauche pulmonaire de l'embryon de poulet: étude ultra-structurale des inclusions granulaires et lamellaires. Z. Anat. Entwickl.-Gesch. 138, 111–126 (1972)

    Google Scholar 

  • Mathan, M., Hermos, J. A., Trier, J. S.: Structural features of the epithelo-mesenchymal interface of rat duodenal mucosa during development. J. Cell Biol. 52, 577–588 (1972)

    Google Scholar 

  • Millonig, G.: A modified procedure for lead staining of thin sections. J. biophys. biochem. Cytol. 11, 736–739 (1961)

    Google Scholar 

  • Noack, W., Zimmermann, B., Merker, H. J.: Elektronenmikroskopische Untersuchungen an embryonalen Rattenlungen (Tag 15) in der Gewebeskultur. Z. Anat. Entwickl.-Gesch. 132, 325–338 (1970)

    Google Scholar 

  • Noack, W.: Das Elektronenmikroskopische Bild des Lungenepithels von Rattenembryonen von Tag 16 bis zur Geburt. Acta anat. (Basel) 79, 445–465 (1971)

    Google Scholar 

  • O'Hare, K. H., Sheridan, M. N.: Electron microscopic observations on the morphogenesis of the albino rat lung with special reference to pulmonary epithelial cells. Amer. J. Anat. 127, 818–205 (1970)

    Google Scholar 

  • O'Hare, K. H., Townes, P. L.: Morphogenesis of albino rat lung: an autoradiographic analysis of the embryological origin of the type II pulmonary epithelial cells. J. Morph. 132, 69–82 (1970)

    Google Scholar 

  • Parry, E. W.: Some electron microscopic observations on the mesenchymal structure of full term umbilical cord. J. Anat. (Lond.) 107, 505–518 (1970)

    Google Scholar 

  • Perdue, J. F.: The distribution, ultrastructure and chemistry of microfilaments in cultured chick embryo fibroblasts. J. Cell Biol. 58, 265–283 (1973)

    Google Scholar 

  • Pexieder, T.: The tissue dynamics of heart morphogenesis. I. The phenomena of cell death. A identification and morphology. Z. Anat. Entwickl.-Gesch. 137, 270–284 (1972)

    Google Scholar 

  • Rash, J. E., Shay, V. W., Biesele, J. J.: Cilia in cardiac differentiation. J. Ultrastruct. Res. 29, 470–484 (1969)

    Google Scholar 

  • Ross, R.: The connective tissue fiber forming cell. In: Treatise on collagen. Vol. 2, Biol. of Coll. Part A, ed. B. S. Gould, p. 1–82. London-New York: Academic Press 1968

    Google Scholar 

  • Ross, R.: Smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J. Cell Biol. 50, 172–186 (1971)

    Google Scholar 

  • Ryan, G. B., Cliff, W. J., Gabbiani, G., Irlé, C., Montandon, D., Statkov, P. R., Majno, G.: Myofibroblasts in human granulation tissue. Human Path. 5, 55–68 (1974)

    Google Scholar 

  • Ryan, S. F.: The structure of interalveolar septum of the mammalian lung. Anat. Rec. 165, 467–483 (1969)

    Google Scholar 

  • Salzgeber, B., Wolff, E.: Experimental production of malformations of the limb by means of chemical substances. Int. Rev. exp. Path. 3, 329–363 (1964)

    Google Scholar 

  • Sorokin, S.: Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363–377 (1962)

    Google Scholar 

  • Sorokin, S.: Recent work on developing lung. In: Organogenesis, ed. Dehard and Ursprung, p. 467–491. New York: Holt, Rinehart and Winston 1965

    Google Scholar 

  • Suzuki, Y.: The structural differentiation of the alveolar lining cells. II. On the structural components of the alveolar wall during the process of development. Okajimas Folia Anat. 42, 149–169 (1966)

    Google Scholar 

  • Van Furth, R., Cohn, Z. A.: The origin and kinetics of mononuclear phagocytes. J. exp. Med. 128, 415–436 (1968)

    Google Scholar 

  • Wheatley, B. M.: Cilia in cell-cultured fibroblasts. III. Relationship between mitotic activity and cilia frequency in mouse 3T6 fibroblasts. J. Anat. (Lond.) 110, 367–382 (1971)

    Google Scholar 

  • Williams, G.: The late phases of wound healing: histological and ultrastructural studies of collagen and elastic tissue formation. J. Path. 102, 61–68 (1970a)

    Google Scholar 

  • Williams, G.: The pleural reactions to injury: a histological and electron optical study with special reference to elastic tissue formation. J. Path. 100, 1–7 (1970b)

    Google Scholar 

  • Wolff, E.: Les facteurs de la différenciation embryonnaire. Rev. franç. Etud. clin. Biol. 12, 223–237 (1967)

    Google Scholar 

  • Woodside, G. L., Dalton, A. J.: The ultrastructure of lung tissue from newborn and embryo mice. J. Ultrastruct. Res. 2, 28–54 (1958)

    Google Scholar 

  • Wynn, R. M.: Derivation and ultra-structure of so-called Hofbauer cells. Amer. J. Obstet. Gynec. 97, 235–248 (1967)

    Google Scholar 

  • Yasuda, H.: Electron microscopic cyto-histopathology (IV) A study of normal and fetus lung in mammals as revealed by electron microscopy. Acta path. jap 8, 189–213 (1958)

    Google Scholar 

  • Yu, S. Y., Sun, C. N.: Lipid accumulation and differentiation of septal cells in postnatal development of lungs. In: 6th Int. Congress for Electr. Micr. Kyoto 1966, p. 593–594 (1966)

  • Yu, S. Y., Sun, C. N.: Septal cells and postnatal development of rat lungs. Electron microscopic and biochemical studies. Cytologia 37, 399–414 (1972)

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Laval University Medical School, Québec City, Québec

    A. J. Collet

  2. Laboratoire d'Anatomie Microscopique, CEGEP, Ste-Foy, Québec, Canada

    G. Des Biens

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  1. A. J. Collet
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  2. G. Des Biens
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This work has been supported by the Medical Research Council of Canada (Grant No ME 3388).

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Collet, A.J., Biens, G.D. Evolution of mesenchymal cells in fetal rat lung. Anat. Embryol. 147, 273–292 (1975). https://doi.org/10.1007/BF00315076

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