Ultrastructure of neoblasts in microturbellaria: Significance for understanding stem cells in free-living platyhelminthes

Invertebrate Reproduction and Development

Volumn 35, Issue 2, 1999, Pages 127-140

  Rieger, Reinhard M ^a   Legniti, Alexander ^a   Ladurner, Peter ^a   Reiter, Dietmar ^a   Asch, Esther ^a   Salvenmoser, Willibald Sal ^a   SchÜrmann, Wolfgang ^b   Peter, Roland ^b  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b UNIVERSITY OF SALZBURG   (Austria)

Author keywords

Heterochromatin; Neoblasts; Platyhelminthes; Stem cells; Ultrastructure

Indexed keywords

EID: 0032958788     PISSN: 07924259     EISSN: None     Source Type: Journal    
DOI: 10.1080/07924259.1999.9652376     Document Type: Article

References (68)

1. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J. D., 1994. Molecular Biology of the Cell, 3rd ed Garland, New York
2. Auladell, C., Garcia-Valero, J., and Baguñà, J., 1993. Ultra-structural localization of RNA in the chromatoid bodies of undifferentiated cells (neoblasts) in planarians by the Rnase-Gold complex technique. J. Morph., 216:319–326.
3. Ax, P., 1995. Das System der Metazoa I Ein Lehrbuch der phylogenetischen Systematik. Gustav Fischer, Stuttgart, Jena, New York
4. Ax, P., 1996. Multicellular Animals A New Approach to the Phylogenetic Order in Nature. Springer, Berlin, Heidelberg, New York
5. Baguñà, J., 1981. Planarian Neoblast. Nature, 290:14–15.
6. Baguñà, J., 1998. Cellular and Molecular Basis of Regeneration:From Invertebrates to Humans Edited by:Feretti, P., and Gtraudie, J., 135–165. New York:Wiley. Planarians. In
7. Baguñà, J., and Boyer, B. C., 1990. “ Descriptive and experimental embryology of the Turbellaria:Present knowledge, open questions and future trends ”. In Experimental Embryology in Aquatic Plants and Animals, NATO ASI Series A:195 Edited by:Marthy, H., 95–128.
8. Baguñà, J., Romero, R., Salò, E., Collet, J., Auladell, C., Ribas, M., Ruitort, M., Garcia-Fernández, J., Burgaya, F., and Bueno, D., 1990. Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians, NATO ASI Series A 129–162. Experimental Embryology in Aquatic Plants and Animals, 195
9. Baguñà, J., Salò, E., Romero, R., Garcia-Fernández, J., Bueno, D., Muñoz-Marmol, A. M., Bayascas-Ramirez, J. R., and Casali, A., 1994. Regeneration and pattern formation in planarians:cells, molecules and genes. Zool. Sci., 11:781–795.
10. Bayascas, J. R., 1997. Castillo, E., Muñoz-Marmol, A.M. and Saló E., Planarian Hox genes:novel patterns of expression during regeneration. Development, 124:141–148.
11. Bayascas, J. R., 1998. Castillo. E. and Saló E., Platyhelminthes have a Hox code differentially activated during regeneration, with genes closely related to those of spiralian protostomes. Dev Genes Evol., 208:467–473.
12. Boyer, B., Henry, J. Q., and Martindale, M. Q., 1996. Dual origins of mesoderm in a basal spiralian:Cell lineage analysis in the polyclad turbellarian Hoploplana inquilina. Dev. Biol., 179:329–338.
13. Boyer, B., Henry, J. Q., and Martindale, M. Q., The cell lineage of the polyclad Hoploplana inquilina. Hydrobiologia, in press
14. Brmsted, H. V., 1969. Planarian Regneration Pergamon Press, Oxford
15. Bueno, D., and Espinosa, L., 1997. Baguñà, J. and Romero, R., Planarian pharynx regeneration in regenerating tail fragments monitored with cell-specific monoclonal antibodies. Dev. Genes Evol., 206:425–434.
16. Carranza, S., 1997. Baguñà, J. and Riutort, M., Are the Platyhelminthes a monophyletic primitive group?. An assessment using 18s rDNA sequences. Mol. Biol. Evol., 14 (5):485–497.
17. Conway-Morris, S., 1993. The fossil record and the early evolution of the Metazoa. Nature, 361:219–225.
18. Ehlers, U., 1985. Das Phylogenetische System der Plathelminthes Gustav Fischer, Stuttgart
19. Ehlers, U., 1992. No mitosis of differentiated epidermal cells in the Plathelminthes:mitosis of intraepidermal stem cells in Rhynchoscolex simplex Leidy, 1851 (Catenulida). Microfauna Marina, 7:311–312.
20. Ehlers, U., 1995. The basic organization of the Plathelminthes. Hydrobiologia, 305:21–26.
21. Ehlers, U., and Sopott-Ehlers, B., Ultrastructure of the subepidermal musculature of Xenoturbella bocki, the adelphotaxon of the Bilateria. Zoomorph., 117 (198) 71–79.
22. Elgin, S. C.R., 1996. Heterochromatin and gene regulation in Drosophila. Curr. Op. Gen. Dev., 6:193–202.
23. Gardner, R. L., and Beddington, R. S.P., 1988. Multi-lineage ‘stem’ cells in the mammalian embryo. J. Cell. Sci. Suppl., 10:11–27.
24. Gilbert, S. F., 1997. Developmental Biology, 5th ed. Sinauer Associates, Sunderland, MA
25. Gremigni, V., 1981. The problem of cell totipotency, dedifferentiation and transdifferentiation in Turbellaria. Hydrobiologia, 84:171–179.
26. Gremigni, V., 1988. Planarian regeneration:An overview of some cellular mechanisms. Zool. Sci., 5:1153–1163.
27. Gustafsson, M. K.S., 1977. Aspects on the cytology and histogenesis in cestodes with special reference to the genus Diphyllobothrium Finland:Åbo Akademi. PhD Thesis
28. Haszprunar, G., 1996. Plathelminthes and Plathelminthomorpha-paraphyletic taxa. J. Zool. Syst. Evol. Res., 34:41–48.
29. Hay, E. D., and Coward, S. J., 1975. Fine structure studies on the Planarian. Dugesia. I. Nature of the “neoblast” and other cell types in noninjured worms. J. Ultrastr. Res., 50:1–21.
30. Hall, F., Morita, M., and Best, J. B., 1986. Neoplastic transformation in the Planarian:I. Carinogenesis and Histopathology. J. Exp. Zool., 240:211–227.
31. Heath, J. K., and Smith, A. G., 1988. Regulatory factors of embryonic stem cells 257–267. J. Cell Sci. Suppl
32. Hooge, M. D., and Tyler, S., 1999. Body-wall musculature of Praeconvoluta tornuva n.sp. and the use of muscle patterns in taxonomy of acoel turbellarians. Invert. Bioi., 118:8–17.
33. Hori, I., 1982. An ultrastructural study of the chromatoid body in planarian regenerative cells. J. Electron. Microsc., 31 (1):63–72.
34. Hori, I., 1997. Cytological approach to morphogenesis in the planarian blastema. II. The effect of neuropeptides. J. Submicrosc. Cytol. Pathol,., 29:91–97.
35. Hyman, L. H., 1951. The Invertebrates. II. Platyhelminthes and Rhynchocoela. The Acoelomate Bilateria New York:McGraw-Hill.
36. Ladumer, P., Mair, G. R., Reiter, D., Salvenmoser, W., and Rieger, R. M., 1997. The serotonergic nervous system of two macrostomid species:recent or ancient divergence?. Invertebr. Biol., 3:178–191.
37. Ladumer, P., Reiter, D., Riedl, D., and Rieger, R. M., 1998. Stem cells in turbellarian development, growth, and regeneration (abstract). Dev. Biol., 198 209
38. Legniti, A., Rieger, R., and Haszprunar, G., 1989. Cellular components in the acoelomate body cavity in the hatchling and the adult of Macrostomum hystricinum (Turbellaria, Macrostomida). Eur. J. Cell Biol. Suppl., 27:49–55.
39. Lord, B. I., and Dexter, T. M., 1988. Stem cells. J. Cell Sci. Suppl., 10 288
40. Morita, M., Best, J. B., and Noel, J., 1969. Electron microscopic studies of planarian regeneration. I. Fine structure of neoblasts in Dugesia dorotocephala. J. Ultrastr. Res., 27:7–23.
41. Morita, M., and Best, J. B., 1984. Electron microscopic studies of planarian regeneration. IV. Cell division of neoblasts in Dugesia dorotocephala. J. Exp. Zool., 229:425–436.
42. Morrison, S. J., Shah, N. M., and Anderson, D. J., 1997. Regulatory mechanisms in stem cell biology. Cell, 88:287–298.
43. Orii, H., Miyamoto, T., Agata, K., and Watanabe, K., 1995. cDNA cloning and partial sequencing of homeobox genes in Dugesia japonica. Hydrobiologia, 305:277–279.
44. Palmberg, I., 1990. Stem cells in microturbellarians, an autoradio-graphic and immunocytochemical study. Protoplasma, 158:109–120.
45. Palmberg, I., 1991. Differentiation during asexual reproduction and regeneration in a microturbellarian. Hydrobiologia, 227:1–10.
46. Pedersen, K. J., 1959. Cytological studies on the planarian neoblast. Z. Zellforsch., 50:799–817.
47. Pedersen, K. J., 1972. Studies on regeneration blastemas of the planarian Dugesia tigrina with special reference to differentiation of the muscle-connective tissue filament system. Roux's Arch. Entwickl.-Mech. Org., 169 (2):134–169.
48. Potten, C. S., 1983. Stem Cells:Their Identification and Characterisation Edited by:Potten, C. S., New York:Churchill-Livingstone.
49. Potten, C. S., and Morris, R. J., 1988. Epithelial stem cells in vivo. J. Cell Sci. Suppl., 10:45–62.
50. Reiter, D., Boyer, B., Ladurner, P., Mair, G., Salvenmoser, W., and Rieger, R., 1996. Differentiation of the body wall musculature in Macrostomurn hystricinum marinum Hoploplana inquilina (Plathelminthes), as models for muscle development in lower Spiralia Roux's Arch. Dev. Biol., 205:410–423.
51. Reuter, M., and Palmberg, I., 1987. An ultrastructural and immunocytochemical study of gastrodermal cell types in Microstomum lineare (Turbellaria, Macrostomida). Acta Zool. (Stockh.), 68:153–163.
52. Rieger, R. M., 1977. “ The relationship of character variability and morphoiogical complexity in copulatory structures of Turbellaria-Macrostomida and Haplopharyngida ”. In The Meiofauna Species in Time and Space, Microfauna Meeresboden Edited by:Sterrer, W., and Ax, P., Vol. 61, 197–216.
53. Rieger, R. M., and Ruppert, E., 1978. Resin embedments of quantitative meiofauna samples for ecological and structural studies—description and application. Mar. Biol., 46:223–235.
54. Rieger, R. M., 1985. “ The phylogenetic status of the acoelomate organization within the Bilateria:a histological perspective ”. In The Origins and Relationships of Lower Invertebrates Edited by:Conway-Morris, S., George, J. D., Gibson, R., and Platt, H. M., 101–122. Oxford:Clarendon Press.
55. Rieger, R. M., and Salvenmoser, W., 1991a. Demonstration of the muscle system in whole mounts of Macrostomum hystricinum (Turbellaria, Macrostomida). Am. Zool., 31 25
56. Rieger, R. M., Tyler, S., Smith, J. P.S., III and Rieger, G. E., 1991b. “ Platyhelminthes:Turbellaria ”. In Platyhelminthes and Nemertinea. Microscopic Anatomy of Invertebrates Edited by:Harrison, F. W., and Bogitsh, B. J., Vol. 3, 7–140. Wiley-Liss.
57. Rieger, R. M., Salvenmoser, W., Legniti, A., Simonsberger, P., Adam, H., and Tyler, S., 1991c. Organization and differentiation of the body-wall musculature in Macrostomum (Turbellaria, Macrostomidae). Hydrobiologia, 227:119–129.
58. Rieger, R. M., Salvenmoser, W., Legniti, A., and Tyler, S., 1994. Phalloidin-rhodamine preparations of Macrostomum hystricinum marinum (Plathelminthes):morphology and postembryonic development of the musculature. Zoomorphology, 114:133–147.
59. Rieger, R. M., and Weyrer, S., 1998. “ The Evolution of the lower Metazoa:Evidence from the phenotype ”. In Molecular Evolution:Towards the Origin of Metazoa. Progr. Mol. Subcell. Biol. Edited by:Müller, W. E.G., 21–43. Berlin Heidelberg, Tokyo:Springer.
60. Salvini-Plawen, L. von, and Splechtna, H., 1979. Zur Homologie der Keimblätter. Zeitschr. Zool. Syst. Evolutionsforsch., 17:10–30.
61. Schürman, W., and Peter, R., 1988. Isolation and cultivation of planarian neoblasts by a novel combination of methods. Fortschr. Zool., 36:111–114.
62. Schürman, W., and Peter, R., 1995. Separation of planarian neoblasts based on density gradient centrifugation. Hydrobiologia, 305 267
63. Spector, D. L., 1996. Nuclear organization and gene expression. Exp. Cell Res., 229:189–197.
64. Thomas, M. B., and Edwards, N. C. 1991. Cnidaria:Hydrozoa In:Microscopic Anatomy of Invertebrates, Vol Edited by:Harrison, F. W., and Westfall, J. A., 91–183. New York:Wiley-Liss. 23
65. Tyler, S., 1981. Development of cilia in embryos of the turbellarian Macrostomum. Hydrobiologia, 84:231–239.
66. Tyler, S., and Hyra, G. S., Patterns of musculature as taxonomic characters for the Turbellaria Acoela. Hydrobiologia, in press
67. Wolffe, A., 1998. Chromatin:Structure and Function, 3rd ed San Diego:Academic Press.
68. Wolpert, L., 1988. Stem cells:a problem in asymmetry. J. Cell Sci., Suppl., 10:1–9.