Wilhelm Roux's archives of developmental biology

, Volume 179, Issue 4, pp 251–273 | Cite as

Scanning electron microscopical observations on epidermal wound healing in the PlanarianDugesia tigrina

  • Knud Jørgen Pedersen
Article

Summary

Epidermal wound healing in regeneratingDugesia tigrina (Planaria) has been studied using scanning electron microscopy (SEM). The normal epidermal surface and its differentiations have been descrebed. Observations on living material reveal the highly dynamic state of the wound in invididual animals and its more or less continously changing size due to the state of activity of the animals. These observations show good agreement with the SEM studies, which allow a clear delineation of cellular details of the wound, the wound margins and the apposing epidermal regions. These details are described. The over-all picture of planarian wound healing that emerges is briefly as follows: Epithelization is characterized by absence of proliferation from the “old” intact epidermis. Variable contraction of smooth muscle cells reduces the wound size to a certain extent. Simultaneously with this and also during a longer period epidermal cells adjacent to the wound are extending and some become highly attenuated. These two processes together are only to a certain degree effective in wound closure because of a definite epidermal cell deficit which is reflected in the emergence of an epidermal wound edge reflecting the maximal contribution of these two processes to an attempt to close the wound. Complete epithelization is effected by the operation of a third mechanism: Recruitment of cell through flow of subjacent “blastemal cells” (including rhabdite-forming cells) along the wound border; these cells subsequently occupy a peripheral position in the wound. This process is supplemented by cell immigration and insertion into the adjacent old epidermis and in the wound cell sheet. Rhabdite-forming cells contribute predominantly to this process. Eventually integration between old epidermal cells and the newly recruited cells which differentiate into epidermal cells results in final epithelization. Complete wound healing is based on interactions between the epidermal cell system and the regenerating subepidermal membrane-connective tissue filament-muscle cell system.

Key words

Planaria Regeneration Would healing Differentiation Epidermis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson Gordon, M.: Observations of epidermal differentiation in regeneration. Virg. J. Sci.13, 248 (1962).Google Scholar
  2. Bandier, J.: Histologische Untersuchungen über die Regeneration von Landplanarien. Arch. Entwickl.-Mech. Org.135, 316–348 (1936).Google Scholar
  3. Bard, J. B. L., Hay, E. D., Meller, S. M.: Formation of the endothelium of the avian cornea: A study of cell movement in vivo. Develop. Biol.42, 334–361 (1975)PubMedGoogle Scholar
  4. Bartsch, O.: Die Histiogenese der Planariengewebe. Arch. Mikr. Anat.99, 187–221 (1923)Google Scholar
  5. Betchaku, T.: Isolation of planarian neoblasts and their behaviorin vitro with some aspects of the mechanism of the formation of regeneration blastema. J. exp. Zool.164, 407–434 (1967).PubMedGoogle Scholar
  6. Betchaku, T.: The cellular mechanism of the formation of a regeneration blastema of fresh-water PlanariaDugesia dorotocephala. I. The behavior of cells in a tiny body fragment isolatedin vitro. J. exp. Zool.174, 253–280 (1970)PubMedGoogle Scholar
  7. Bowen, I. D., Ryder, T. A.: The fine structure of the planarianPolycelis tenius (Iijima). III. The epidermis and external features. Protoplasma (Wien)70, 381–392 (1974)Google Scholar
  8. Brøndsted, H. V.: Planarian regeneration. Oxford: Pergamon Press 1969Google Scholar
  9. Burke, J. M.: Wound healing inEisenia foetida (Oligochaeta) I. Histology and3H-thymidine radioautography of the epidermis. J. exp. Zool.188, 49–64 (1974a)PubMedGoogle Scholar
  10. Burke, J. M.: Wound healing inEisenia foetida (Oligochaeta) II. A fine structural study of the role of the epidermis. Cell Tiss. Res.154, 61–82 (1974b)Google Scholar
  11. Coward, S. J., Vitale-Calpe, R. O.: Behaviorally significant surface specializations of the planarianDugesia dorotocephala. J. Biol. Psychol.14, 3–10 (1971)Google Scholar
  12. Coward, S. J., Bennett, C. E., Hazlehurst, B. L.: Lysosomes and lysosomal enzyme activity in the regenerating planarian; evidence in support of dedifferentiation. J. exp. Zool.189, 133–146 (1974)PubMedGoogle Scholar
  13. Dubois, F.: Contribution à l'étude de la migration des cellules de régénération chez les planaires dulcicoles. Bull. biol.83, 213–283 (1949).Google Scholar
  14. Freisling, M., Reisinger, E.: Zur Genese und Physiologie von Restitutionskörpern aus Planarien-Gewebsbrei. Wilhelm Roux' Arch. Entwickl.-Mech. Org.150, 581–606 (1958)Google Scholar
  15. Goldman, R. D., et al.: Fibrillar systems in cell motility. In: Locomotion of tissue cells. Ciba Foundation Symp. 14 (New series). Amsterdam: Elsevier 1973.Google Scholar
  16. Graff, L. v.: In: Bronn's Klassen und Ordnungen des Tier-Reichs 4. Ic. II. Leipzig: C. F. Winter 1912–1917.Google Scholar
  17. Gustafson, T., Wolpert, L.: Cellular movement and contact in sea urchin morphogenesis. Biol. Rev. (Camb.)42, 442–498 (1967)Google Scholar
  18. Hay, E. D., Coward, S. J.: Fine structure studies on the planarianDugesia. I. Nature of the “neoblast” and other cell types in nonijured worms. J. Ultrastruct. Res.50, 1–21 (1975)PubMedGoogle Scholar
  19. Ichikawa, A., Ishii, S.: Morphological and histochemical studies on regeneration in a fresh-water planarian,Dendrocoelopsis lacteus. J. Fac. Sc. Hokkaido Univ. Ser.6, Zool.14, 595–606 (1961)Google Scholar
  20. Klima, J.: Elektronenmikroskopische Studien über der Tricladen (Turbellaria). Protoplasma (Wien)54, 101–162 (1961)Google Scholar
  21. Kolmayer, S., Stéphan-Dubois, F.: Néoblastes et limitation du pouvoir de régénération céphalique chez la planaireDendrocoelum lacteum. J. Embryol. exp. Morph.8, 376–386 (1960)PubMedGoogle Scholar
  22. Lang, P.: Über Regeneration bei Planarien. Arch. mikr. Anat.97, 361–426 (1912)Google Scholar
  23. Lender, T.: Factors in morphogenesis of regenerating fresh-water Planaria. In: Abercrombie, M., and J. Brachet (eds.). Advanc. Morphogenes.2, 305–331 (1962)Google Scholar
  24. Löfberg, J.: Preparation of amphibian embryos for scanning electron microscopy of the functional pattern of epidermal cilia. Zoon2, 3–11 (1974a)Google Scholar
  25. Löfberg, J.: Apical surface topography of invaginating and noninvaginating cells. A scanningtransmission study of amphibian neurulae. Develop. Biol.36, 311–329 (1974b)PubMedGoogle Scholar
  26. MacRae, E. K.: The fine structure of sensory receptor processes in the auricular epithelium of the planarian,Dugesia tigrina. Z. Zellforsch.82, 479–494 (1967)PubMedGoogle Scholar
  27. Maibach, H. I., Rovee, D. T.: Epidermal wound healing. Year Book Med. Publ. 1972.Google Scholar
  28. Morita, M., Best, J. B.: Elektron microscopic studies on planarian regeneration. II. Changes in epidermis during regeneration. J. exp. Zool.187, 345–374 (1974)PubMedGoogle Scholar
  29. Murray, M. R.: The cultivation of$planarian tissuesin vitro. J. exp. Zool.47, 467–499 (1927)Google Scholar
  30. Nelson, C. A., Revel, J.-P.: Scannmng electron microscopic study of cell movements in the corneal endothelium of the avian embryo. Develop. Biol.42, 315–337 (1975)PubMedGoogle Scholar
  31. Nørrevang, A., Wingstrand, K. G.: On the occurrence and structure of choanocyte-like cells in some echinoderms. Acta Zool.,Stockh.)51, 249–274 (1970)Google Scholar
  32. Odland, G., Ross, R.: Luman wound repair. I. Epidermal$regeneration. J. Cell Biol.39, 135–151 (1968)PubMedGoogle Scholar
  33. Pedersen, K. J.: Studies on the nature of planarian connective tissue. Z. Zellforsch.53, 569–608 (1961a)Google Scholar
  34. Pedersen, K. J.: Studier over ferskvandstricladernes cytologi (with an English summary). Copenhagen: Munksgaard 1961bGoogle Scholar
  35. Pedersen, K. J.: Studies on regeneration blastemas of the planarianDugesia tmgrina with special refevence to differentiation of the muscle-connective tissue filament system. Wilhelm Roux' Arch. Entwickl.-Mech. Org.169, 134–169 (1972)Google Scholar
  36. Pedersen, K. J.: In preparationGoogle Scholar
  37. Platzer, I.: Zur Ultrastruktur von Planarienrestitutionskörpern. Ein Beitrag zum Syncytiumproblem. Protoplasma (Wien)60, 34–60 (1965)Google Scholar
  38. Reese, D. H.: An autoradiographic study of the origin of regenerated epidermis, acidophilic gland cells and pharynx in the planarianDugesia dorotocephala. Thesis, Univ. Maryland 1964Google Scholar
  39. Reisinger, E., Kelbetz, S.: Feinbau und Entladungsmechanisms der Rhabditen. Z. wiss. Mikr.65, 472–508 (1964)PubMedGoogle Scholar
  40. Ross, R.: The fibroblast and wound repair. Biol. Rev. (Camb.)43, 51–96 (1968)Google Scholar
  41. Schmidt, A. J.: Cellular biology of vertebrate regeneration and repair. Chicago: Chicago University Press 1968Google Scholar
  42. Sharov, I. I. Cit. in: Vorontsova, M. A., Liosner, L. D.: Asexual propagation and regeneration. London: Pergamon Press 1960Google Scholar
  43. Skaer, R. J.: Some aspects of the cytology ofPolycelis nigra. Quart. J. micr. Sci.102, 295–317 (1961)Google Scholar
  44. Skaer, R. J.: The origin and continous replacement of epidermal cells in the planarianPolycelis tenuis (Iijima). J. Embryol. exp. Morph.13, 129–139 (1965)PubMedGoogle Scholar
  45. Spiegelman, M., Dudley, P. L.: Morphological stages of regeneration in the planarianDugesia tigrina: A light and electron microscopic study. J. Morph.139, 155–184 (1973)Google Scholar
  46. Spooner, B. S.: Morphogenesis of vertebrate organs. In: Lash, J., Whittaker, J. R.: Concepts of development. Stamford: Sinauer Assoc., Inc. 1974Google Scholar
  47. Stevens, N. M.: Notes on regeneration inPlanaria lugubris. Arch. Entw.-Mech. Org.13, 396–409 (1902)Google Scholar
  48. Teshirogi, W.: Dynamic morphological change and time-table during the regeneration of the turbellarianBdellocephala brunnea. Sc. Rep. Fac. Lit. Sc. Hirosaki Univ.9, 21–48 (1962)Google Scholar
  49. Trinkaus, J. P.: Surface activity and locomotion ofFundulus deep cells during blastula and gastrual stages. Develop. Biol.30, 68–103 (1973)Google Scholar
  50. Török, L. J.: Experimental contributions to the regenerative capacity ofDugesia (=Euplanaria) lugubris O. Schm. Acta Biol. Sci. hung.9, 79–98 (1958)Google Scholar
  51. Török, L. J., Röhlich, P.: Contribution to the fine structure of the epidermis ofDugesia lugubris O. Schm. Acta biol. Sci. hung.10, 23–48 (1959)Google Scholar
  52. Verhoef, A. M.: The mitotic activity during the regeneration ofPolycelis nigra. Proc. kon. ned. Akad. Wet.49, 548–553 (1946)Google Scholar
  53. Wessells, N. K., et al.: Microfilaments in cellular and developmental processes. Science (Wash. D.C.)171, 135–143 (1971)Google Scholar
  54. Wetzel, B. K.: Studies on the fine structure of regeneratingDugesia tigrina (Girard). Thesis Harvard University 1961Google Scholar
  55. Wolff, E.: Recent researches on the regeneration of Planaria. In: Rudnick, D. (ed.): Regeneration. New York: The Ronald Press 1962Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • Knud Jørgen Pedersen
    • 1
  1. 1.Institute of General ZoologyUniversity of CopenhagenCopenhagen ØDenmark

Personalised recommendations