J Appl Biomed 2:21-35, 2004
The significance of stem cells in free-living flatworms: one common source for all cells in the adult
- 1 Department of Genetics and General Biology, University of Salzburg, Salzburg, Austria
- 2 Department of Zoology and Limnology, University of Innsbruck, Innsbruck, Austria
A survey of the current knowledge on stem cells and cell proliferation in turbellarians is presented, with special focus on recent results obtained by the authors when studying cell kinetics and cultivating neoblasts from various species. Differentiated somatic cells do not divide in flatworms. In these animals neoblasts constitute a proliferative compartment. These cells are rather uniform when viewed through a light microscope, but constitute a heterogeneous population comprising actual stem cells, progenitors and early differentiation stages. Cell kinetics were monitored by the incorporation of 5-bromo-2'-deoxyuridine and by immunocytochemical staining for mitoses in the marine microturbellarians Macrostomum, Microstomum and Convolutriloba. Distribution patterns of proliferating cells within the body were documented, and a tentative interpretation of the differences observed is given. Correlations to the nervous system and the mode of reproduction seem to exist. To analyse neoblasts quantitatively and establish primary cultures, neoblasts from the freshwater planarians (triclads) Dugesia and Schmidtea were isolated, purified and subjected to various culture conditions, with the ultimate but not yet achieved goal of establishing a permanent stem cell line. The role of stem cells in flatworms is compared with the situation in mammals, with special focus on embryogenesis, germline and strategies of cell renewal.
Keywords: BrdU labelling; cell cultures; cell proliferation; neoblasts; germline; stem cells
Received: October 24, 2003; Published: March 31, 2004 Show citation
References
- Åkesson B., R. Gschwentner, J. Hendelberg, P. Ladurner, J. Müller, R. Rieger: Fission in Convolutriloba longifissura : asexual reproduction in acoelous turbellarians, revisited. Acta Zool. 82: 231-239, 2001.
Go to original source...
- Asami M., T. Nakatsuka, T. Hayashi, K. Kou, H. Kagawa, K. Agata: Cultivation and characterization of planarian neuronal cells isolated by fluorescence activated cell sorting (FACS). Zool. Sci. 19: 1257-1285, 2002.
Go to original source...
Go to PubMed...
- Auladell C., J. Garcia-Valero, J. Baguñà: Ultrastructural localization of RNA in the chromatoid bodies of undifferentiated cells (neoblasts) in planarians by the RNase-gold complex technique. J. Morph. 216: 319-326, 1993.
Go to original source...
Go to PubMed...
- Baguñà J.: Planarians. In P. Ferretti and J. Géraudie (eds.): Cellular and Molecular Basis of Regeneration: From Invertebrates to Humans. J. Wiley and Sons, Chichester, New York etc., 1998, pp. 135-165.
- Baguñà J., E. Saló, C. Auladell: Regeneration and pattern formation in planaria. III. Evidence that neoblasts are totipotent cells and the source of blastema cells. Development 107: 77-86, 1989.
Go to original source...
- Baguñà J., E. Saló, R. Romero, J. García-Fernàndez, D. Bueno, A.M. Muñoz-Marmol, J.R. Bayascas-Ramirez, A. Casali: Regeneration and pattern formation in planarians: cells, molecules and genes. Zool. Sci. 11: 781-795, 1994.
- Behensky C., W. Schürmann, R. Peter: Quantitative analysis of turbellarian cell suspensions by fluorescent staining with acridine orange, and video microscopy. Belg. J. Zool. 131 (Supplement 1): 131-136, 2001.
- Betchaku T.: Isolation of planarian neoblasts and their behavior in vitro with some aspects of the mechanism of the formation of regeneration blastema. J. Exp. Zool. 164: 407-434, 1967.
Go to original source...
Go to PubMed...
- Brøndsted H.V.: Planarian Regeneration. Pergamon Press, Oxford/London etc., 1969, pp. vii+276.
- Buchner E. and R. Peter: Influences of ionizing radiation on regeneration and neoblasts (stem cells) in the planarian Dugesia tahitiensis (Turbellaria: Tricladida Paludicola). In J. Berger (ed.): Cells IV. Kopp Publ., Èeské Budìjovice 2002, p. 116.
- de Haan G.: Hematopoietic stem cells: self-renewing or aging? Cells Tissues Organs 171: 27-37, 2002.
Go to original source...
Go to PubMed...
- Ehlers U.: The Phylogenetic System of the Platyhelminthes (In German). G. Fischer, Stuttgart, 1985, pp. 317.
- Gremigni V.: The problem of cell totipotency, dedifferentiation and transdifferentiation in Turbellaria. Hydrobiologia 84: 171-179, 1981.
Go to original source...
- Gremigni V.: Planarian regeneration: an overview of some cellular mechanisms. Zool. Sci. 5: 1153-1163, 1988.
- Gschwentner R., P. Ladurner, K. Nimeth, R. Rieger: Number and distribution of S-phase and mitotic cells in Convolutriloba longifissura (Platyhelminthes: Acoela). Cell Tissue Res. 304: 401-408, 2001.
Go to original source...
Go to PubMed...
- Gustafsson M.K.S.: The cells of a cestode. In M.K.S. Gustafsson and M. Reuter (eds.): The early brain. Åbo Academy Press, Åbo 1990: pp. 13-44.
- Keller J.: The asexual reproduction of the freshwater turbellarians (In German). Jen. Zeitschr. Naturwissensch. 28: 370-407, 1894.
- Kirchhof N., F. Harder, S. Petrovic, S. Kreutzfeldt, C. Schmittwolf, M. Dürr, J. Kirsten, B. Mühl, A. Merkel, A.M. Müller: Developmental potential of hematopoietic and neural stem cells: unique or all the same? Cells Tissues Organs 171: 77-89, 2002.
Go to original source...
Go to PubMed...
- Ladurner P., D. Reiter, D. Riedl, R.M. Rieger: Stem cells in turbellarian development, growth and regeneration. Dev. Biol. 198: 209, 1998.
- Ladurner P., R. Rieger, J. Baguñà: Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: a bromodeoxyuridine analysis. Dev. Biol. 226: 231-241, 2000.
Go to original source...
Go to PubMed...
- Le Moigne A.: Study of the embryonic development of Polycelis nigra (triclad turbellarian) (In French). Bull. Soc. Zool. Fr. 88: 403-422, 1963.
- Loeffler M. and I. Roeder: Tissue stem cells: definition, plasticity, heterogeneity, self-organization and models - a conceptual approach. Cells Tissues Organs 171: 8-26, 2002.
Go to original source...
Go to PubMed...
- Morita M. and J.B. Best: Electron microscopic studies of planarian regeneration. IV. Cell division of neoblasts in Dugesia dorotocephala. J. Exp. Zool. 229: 425-436, 1984.
Go to original source...
- Morrison S.J., N.M. Shah, D.J. Anderson: Regulatory mechanisms in stem cell biology. Cell 88: 287-298, 1997.
Go to original source...
Go to PubMed...
- Newmark P.A. and A. Sánchez Alvarado: Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 220: 142-155, 2000.
Go to original source...
Go to PubMed...
- Palmberg I.: Stem cells in microturbellarians. An autoradiographic and immunocytochemical study. Protoplasma 158: 109-120, 1990.
Go to original source...
- Pedersen K.J.: Morphogenetic activities during planarian regeneration as influenced by trimethylene melamine. J. Embryol. Exp. Morphol. 6: 308-334, 1958.
Go to original source...
Go to PubMed...
- Pedersen K.J.: Cytological studies on planarian neoblasts. Z. Zellforsch. 50: 799-817, 1959.
Go to original source...
Go to PubMed...
- Peter R.: Experimental systems for studying regeneration processes: Turbellarians as model organisms with a stem cell system (In German). Ber. nat.-med. Verein Innsbruck 88: 287-350, 2001.
- Peter R.: A totipotent proliferative compartment: the unique stem cell strategy of flatworms. In J. Berger (ed.): Cells IV. Kopp Publ., Èeské Budìjovice 2002, pp. 31-40.
- Peter R., P. Ladurner, R.M. Rieger: The role of stem cell strategies in coping with environmental stress and choosing between alternative reproductive modes: Turbellaria rely on a single cell type to maintain individual life and propagate species. Marine Ecology 22: 35-51, 2001.
Go to original source...
- Rieger R.M., A. Legniti, P. Ladurner, D. Reiter, E. Asch, W. Salvenmoser, W. Schürmann, R. Peter: Ultrastructure of neoblasts in microturbellaria: significance for understanding stem cells in free-living Platyhelminthes. Invertebr. Reprod. Dev. 35: 127-140, 1999.
Go to original source...
- Saló E. and J. Baguñà: Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. J. Embryol. Exp. Morphol. 83: 63-80, 1984.
Go to original source...
Go to PubMed...
- Saló E. and J. Baguñà: Regeneration in planarians and other worms: new findings, new tools and new perspectives. J. Exp. Zool. 292: 528-539, 2002.
Go to original source...
Go to PubMed...
- Sánchez Alvarado A.S. and P.A. Newmark: Double-stranded RNA disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. USA 96: 5049-5054, 1999.
Go to original source...
Go to PubMed...
- Sauzin-Monnot M.J.: Ultrastructural study of the neoblasts of Dendrocoelum lacteum during regeneration (In French). J. Ultrastruct. Res. 45: 206-222, 1973.
Go to original source...
Go to PubMed...
- Schürmann W. and R. Peter: Planarian cell culture: a comparative review of methods and an improved protocol for primary cultures of neoblasts. Belg. J. Zool. 131 (Suppl. 1): 123-130, 2001.
- Schürmann W. and R. Peter: Primary cultures of neoblasts (stem cells) from the planarians Dugesia tahitiensis and Schmidtea polychroa (Platyhelminthes: Turbellaria - Tricladida). J. appl. Biomed. 1 (Suppl. 1): S28-29, 2003.
- Schürmann W., S. Betz, R. Peter: Separation and subtyping of planarian neoblasts by density-gradient centrifugation and staining. Hydrobiologia 383: 117-124, 1998.
Go to original source...
- Shibata N., Y. Umesono, H. Orii, T. Sakurai, K. Watanabe, K. Agata: Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of vasa planarians. Dev. Biol. 206: 73-87, 1999.
Go to original source...
Go to PubMed...
- Theise N.D., S. Badve, R. Saxena, O. Henegariu, S. Sell, J.M. Crawford, D.S. Krause: Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31: 235-240, 2000.
Go to original source...
Go to PubMed...
- Theise N.D., M. Nimmakayalu, R. Gardner, P.B. Illei, G. Morgan, L. Teperman, O. Henegariu, D.S. Krause: Liver from bone marrow in humans. Hepatology 32: 11-16, 2000.
Go to original source...
Go to PubMed...
- Vescovi A., A. Gritti, G. Cossu, R. Galli: Neural stem cells: plasticity and their transdifferentiation potential. Cells Tissues Organs 171: 64-76, 2002.
Go to original source...
Go to PubMed...
- Weismann A.: The germ plasm. A theory of heredity (In German). Fischer, Jena 1892.
Go to original source...
- Weissman I.L.: Stem cells: units of development, units of regeneration, and units in evolution. Cell 100: 157-168, 2000.
Go to original source...
Go to PubMed...
- Wikgren B.-J. and C.M. Knuts: Growth of subtegumental tissue in cestodes by cell migration. Acta Acad. Aboensis Ser. B 30: 1-6, 1970.