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Cellular and Molecular Neurobiology

, Volume 16, Issue 5, pp 591–616 | Cite as

Neuronal signal substances in asexual multiplication and development in flatworms

  • Maria Reuter
  • Margaretha Gustafsson
Article

Summary

  1. 1.

    The phenomenon of asexual multiplication is rare in the animal kingdom. It occurs, however, in all main flatworm taxa. Flatworms are characterized by an extensive versatility, ranging from the different types of asexual multiplication to the different orthogonal plans for the nervous system. The role of the nervous system in the asexual multiplication taking place in flatworms is pointed out and discussed.

     
  2. 2.

    Immunocytochemical studies of the changes in the flatworm neuroanatomy show that the nervous system, particularly the main never cords, has a central role during asexual development.

     
  3. 3.

    Antibodies to different neuronal substances yield different immunoreactivity patterns and develop according to different time schedules. Serotoninergic nervous elements seem to have a leading role.

     
  4. 4.

    Substances produced by the nervous system influence fissioning and subsequent regeneration in free-living flatworms in the following ways. (a) A function as a wound hormone has been suggested for the neuropeptide RF-amide. (b) Mitogenic effects have been shown for several biogenic amines and neuropeptides. (c) Inhibitory roles are suggested for somatostatin and melatonin in connection with cell proliferation respective fissioning.

     
  5. 5.

    Growth factors have been observed both in free-living and parasitic flatworms.

     
  6. 6.

    Cells reactive to antibodies against epidermal growth factor increase in number in parallel with increases in mitotic activity in the gull tapeworm and occur in regions with high mitotic activity. A correlation between these two phenomena is suggested.

     

Key Words

flatworms asexual multiplication development neuronal signal substances 

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References

  1. Ax, P., and Schulz, E. (1959). Ungeschlechtiche Fortpflanzung durch Paratomie bei acoelen Turbellarien.Biol. Zentralblan 78:613–621.Google Scholar
  2. Bagunñà, J., Saló, E., and Romero, R. (1989). Effects of activators and antagonists of the neuropeptides substance P and substance K on cell proliferation in planarians.Int. J. Dev. Biol. 33:261–264.PubMedGoogle Scholar
  3. Baguñà, J., Romero, R., Saló, E., Collet, J., Auladell, C., Ribas, M., Riutort, M., García-Fernandez, J., Burgaya, F., and Bueno, D. (1990). Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. In (H. Marthy, Ed.),Experimental Embryology in Aquatic Plants and Animals, Plenum Press, New York, pp. 129–162.Google Scholar
  4. Barton, C. L., Halton, D. W., Shaw, C., Maule, A. G., and Johnson, C. F. (1993). An immunocytochemical study of putative neurotransmitters in the metacercarias of two strigeoid trematodes from rainbow trout (Oncorhynchus mykiss).Parasit. Res. 79:389–396.Google Scholar
  5. Bautz, A., and Schilt, J. (1986). Somatostatin-like peptide and regeneration capacities in planarians.Gen. Comp. Endocrinol.,64:267–272.PubMedGoogle Scholar
  6. Best, J. B., Goodman, A. B., and Pigon, A. (1969). Fissioning in planarians: Control by the brain.Science 164:565–566.PubMedGoogle Scholar
  7. Bråten, T. (1966). Studies of the helminth fauna of Norway. VII. Growth, fecundity, and fertility ofDiphyllobothrium norwegicum Vik, (Cestoda) in the golden hamster.Nyt Mag. Zool. (Oslo) 13:39–51.Google Scholar
  8. Bylund, G. (1969) Experimentell undersökning avDiphyllobothrium dendriticum (=D. norwegicum) från norra Finland.Information 10:3–17.Google Scholar
  9. Fairweather, I., Macartney, G. A., Johnston, C. G., Halton, D. W., and Buchanan, K. D. (1988). Immunocytochemical demonstration of 5-hydroxythryptamine (serotonin) and vertebrate neuropeptides in the nervous system of excysted cysticercoid larvae of the rat tapewormHymenolepis diminuta.Parasitol. Res. 74:371–479.PubMedGoogle Scholar
  10. Grahn, M., Maule, A. G., Elo, I., Shaw, C., Reuter, M., and Halton, D. W. (1995). Antigenicity to neuropeptide F (NPF) in Stenostomum leucops andMicrostomum lineare.Hydrobiologia 305:307–308.Google Scholar
  11. Grimmelikhuijzen, C. J. P. (1985). Antisera to the sequence Arg-Phe-amide visualize neuronal centralization in hydroid polyps.Cell Tissue Res. 241:171–182.Google Scholar
  12. Grothe, C., Zachman, K., and Unsicker, K. (1991). Basic FGF-like immunoreactivity in the developing and adult rat brain stem.J. Comp. Neurol. 305:328–336.PubMedGoogle Scholar
  13. Gustafsson, M. K. S. (1976). Observations on the histogenesis of nervous tissue inDiphyllobothrium dendriticum Nitzsch, 1824 (Cestoda, Pseudophyllidea).Z. Parasitenk. 50:313–321.PubMedGoogle Scholar
  14. Gustafsson, M. K. S. (1984). Synapses inDiphyllobothrium dendriticum (Cestoda). An electron microscopical study.Acta Zool. Fennica 21:167–175Google Scholar
  15. Gustafsson, M. K. S. (1990). The cells of a cestode-Diphyllobothrium dendriticum as a model in cell biology. In (M. K. S. Gustafsson and M. Reuter, (Eds.),The Early Brain. Acta Acad. Aboenis Ser. B 50:13–44.Google Scholar
  16. Gustafsson, M. K. S. (1992). The neuroanatomy of parasitic flatworms.Adv. Neuroimmunol. 2: 267–286.Google Scholar
  17. Gustafsson, M. K. S., and Eriksson, K. (1992). Never ending growth and a growth factor. I. Immunocytochemical evidence for the presence of basic fibroblast growth factor in a tapeworm.Growth Factors 7:327–334.PubMedGoogle Scholar
  18. Gustafsson, M. K. S., and Wikgren, M. C. (1981a). Activation of the peptidergic neurosecretory system inDiphyllobothrium dendriticum (Cestoda: Pseudophyllidea).Parasitiology 83:243–247.Google Scholar
  19. Gustafsson, M. K. S., and Wikgren, M. C. (1981b). Release of neurosecretory material by protrusions of bounding membranes extending through the axolemma, inDiphyllobothrium dendriticum (Cestoda).Cell Tissue Res. 220:473–479.PubMedGoogle Scholar
  20. Gustafsson, M. K. S., and Wikgren, M. C. (1989). Development of immunoreactivity to the invertebrate small cardiac peptide B in the tapewormDiphyllobothrium dendriticum.Parasitol. Res. 75:396–400.PubMedGoogle Scholar
  21. Gustafsson, M. K. S., Jukanen, A. C., and Wikgren, M. C. (1983). Activation of the peptidergic neurosecretory system inDiphyllobothrium dendriticum (Cestoda) at suboptimal temperatures.Z. Parasitenk. 69:279–282.PubMedGoogle Scholar
  22. Gustafsson, M. K. S., Wikgren, M. C., Karhi, T. J., and Schot, L. P. C. (1985). Immunocytochemical demonstration of neuropeptides and serotonin in the tapewormDiphyllobothrium dendriticum.Cell Tissue Res. 240:255–260.PubMedGoogle Scholar
  23. Gustafsson, M. K. S., Lehtonen, M. A. J., and Sundler, F. (1986). F. (1986). Immunocytochemical evidence for the presence of “mammalian” neurohormonal peptides in neurones of the tapewormDiphyllobothrium dendriticum.Cell Tissue Res. 243:41–49.PubMedGoogle Scholar
  24. Gustafsson, M. K. S., Nässel, D., and Kuusisto, A. (1993). Immunocytochemical evidence for the presence of substance P-like peptide inDiphyllobothrium dendriticum.Parasitology 106:83–89.PubMedGoogle Scholar
  25. Gustafsson, M. K. S., Halton, D. W., Maule, A. G., Reuter, M., and Shaw, C. (1994). The gull-tapewormDiphyllobothrium dendriticum and neuropeptide F: An immunocytochemical study.Parasitology 109:599–609.Google Scholar
  26. Gustafsson, M. K. S., Eriksson, K., and Hydén, A. (1995).. Never ending growth and a growth factor. II. Immunocytochemical evidence for the presence of of epidermal growth factor in a tapeworm.Hydrobiologia 305:229–233.Google Scholar
  27. Gustafsson, M. K. S., Fagerholm, H.-P., Halton, D. W., Hanzelova, V., Maule, A. G., Reuter, M., and Shaw, C. (1995b). Neuropeptide and serotonin in the cestode,Proteocephalus exiguus: An immunocytochemical study.Int. J. Parasitol. 25:673–682.PubMedGoogle Scholar
  28. Halton, D. W., Shaw, C., Maule, A. G., and Smart, D. (1994). Regulatory peptides in helminth parasites.Adv. Parasitol. 34:164–227.Google Scholar
  29. Kotikova, E. A. (1986). Comparative characterization of the nervous system of the Turbellaria.Hydrobiologia 132:89–92.Google Scholar
  30. Kotikova, E. A. (1986). Comparative characterization of the nervous system of the Turbellaria.Hydrobiologia 132:89–92.Google Scholar
  31. Kotikova, E. A. (1991). The orthogon of the platyhelminthes and the main trends of its evolution.Proc. Zool. Inst. St. Petersburg 241:88–111 (in Russian).Google Scholar
  32. Krichinskaya, E. B. (1986). Asexual reproduction, regeneration, and somatic embryogenesis in the planarianDugesia tigrina (Turbellaria).Hydrobiologia 132:195–200.Google Scholar
  33. Lender, T. (1974). The role of neurosecretion in freshwater planarians. In (N. W. Riser and M. P. Morse, Eds.),Biology of the Turbellaria, McGraw-Hill, London, pp. 460–475.Google Scholar
  34. Mamkaev, Y. V. (1986). Initial morphological diversity as a criterion deciphering turbellarian phylogeny.Hydrobiologia 122:31–32.Google Scholar
  35. Martelly, I., Franquinet, R., and LeMoigne, A. (1981). Relationships between variations of cAMP, neuromediators and the stimulation of nucleic acid synthesis during planarian (polycelis tenuis) regeneration.Hydrobiologia 84:195–201.Google Scholar
  36. Martelly, I., Moraczewski, J., Franquinet, R., and Castagna, M. (1987). Protein kinase C activity in a fresh water planarian (Dugesia gonocephala).Comp. Biochem. Physiol. 86B:405–409.Google Scholar
  37. Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C., and Fairweather, I. (1990). The serotoninergic, cholinergic and peptidergic components of the nervous system of the monogenean parasite,Diclidophora merlangi: A cytochemical study.Parasitology 100:255–273.PubMedGoogle Scholar
  38. McMichael-Phillips, D., Lewis, J. N., and Thorndyke, M. C. (1991). SALMFamide-, FMRFamide- and serotoninlike mapping in the nervous system of cercariae fromSanguinicola inermis.Regul. Peptides 35:245.Google Scholar
  39. Moraczewski, J. (1977). Asexual reproduction and regeneration ofCatenula (Tuberllaria, Archoophora).Zoomorphologie 88:65–80.Google Scholar
  40. Moraczewski, J. Martelly, I., Franquinet, R., and Castagna, R. (1987). Protein kinase C activity during planarian regeneration.Comp. Biochem. Physiol. 87B:703–707.Google Scholar
  41. Morita, M., and Best, J. B. (1984). Effects of photoperiods and melatonin on planarian asexual reproduction.J. Exp. Zool. 231:273–283.Google Scholar
  42. Nentwig, M. R. (1978). Comparative morphological studies of head development after decapitation and after fission in the planarianDugesia dorotocephala.Trans. Am. Microsc. Soc. 97:297–310.PubMedGoogle Scholar
  43. Niewiadomska, K., and Moczon, T. (1982). The nervous system ofDiplostomum pseudospathaceum Niewiadomska, (Digenea, Diplostomum). I. Nervous system and chaetotaxy in cercaria.Z. Parasitenkd. 68:296–304.Google Scholar
  44. Niewiadomska, K., and Moczon, T. (1984). The nervous system ofDiplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomatidae). II. Structure and development of the nervous system in metacercaria.Z. Parasitenkd. 70:537–548.Google Scholar
  45. Niewiadomska, K., and Moczon, T. (1987). The nervous system ofDiplostomum pseudopathaceum Niewiadomska, 1984 (Trematoda, Diplosotmatidae). III. Structure of the nervous system of the adult stage.Parasitol. Res. 73:46–49.PubMedGoogle Scholar
  46. Palmberg, I. (1991). Differentiation during asexual reproduction and regeneration in a microturbellarian.Hydrobiologia 227:1–10.Google Scholar
  47. Palmberg, I., and Reuter, M. (1983). Asexual reproduction inMicrostomum lineare (Turbellaria). I. An autoradiographic and ultrastructural study.Int. J. Invertebr. Reprod. 6:197–206.Google Scholar
  48. Palmberg, I., and Reuter M. (1990). Neuronal subsets in regeneratingMicrostomum lineare. Immunocytochemistry of FMRF/RF-amide and 5-HT. In (M. K. S. Gustafsson and M. Reuter, Eds.),The Early Brain. Acta Acad. Aboensis 50:147–160.Google Scholar
  49. Pan, J.-Z., Halton, D. W., Shaw, C., Maule, A. G., and Johnston, C. F. (1994). Serotonin (5-HT)- and neuropeptide-immunoreactivities in the intramolluscan stages of three marine trematode parasites.Parasitol. Res. 80:388–395.PubMedGoogle Scholar
  50. Reuter, M. (1987). Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system ofGyrodactylus salaris (Monogenea).Acta Zool. 86:178–193.Google Scholar
  51. Reuter, M. (1994). Substance P immunoreactivity in sensory structures and the central and pharyngeal nervous system ofStenostomum leucops (Catenulida) andMicrostomum lineare (Macrostomida).Cell Tissue Res. 276:173–180.Google Scholar
  52. Reuter, M., and Eriksson, K. (1990). Catecholamines demonstrated by glyoxylic-acid inducedfluorescence and HPLC in some microtubellarians.Hydrobiologia 227:209–219.Google Scholar
  53. Reuter, M., and Gustafsson, M. K. S. (1989). “Neuorendocrine cells” in flatworms-Progenitors to metazoan neurones?Arch. Histol. Cytol. 52:253–263.PubMedGoogle Scholar
  54. Reuter, M., and Gustafsson, M. K. S. (1995). The flatworm nervous system-Pattern and phylogeny. In O. Breidbach and W. Kutsch, Eds.),The Nervous Systems of Invertebrates—An Evolutionary and Comparative Approach. Advances in Life Sciences, Birkhäuser Verlag, Basel, Boston, Berlin.Google Scholar
  55. Reuter, M., and Juusisto, A. (1992). Growth factors in asexually reproducing Catenulida and Macrostomida (Plathelminthes)?Zoomorphology 122:155–166.Google Scholar
  56. Reuter, M., and Palmberg, I. (1983). Asexual reproduction inMicrostromum lineare (Turbellaria). II. The nervous system in the division zone.Int. J. Invertebr. Reprod. 6:207–217.Google Scholar
  57. Reuter, M., and Palmberg, I. (1989). Development and differentiation of neuronal subsets in asexually reproducingMicrostromum lineare. Immunocytochemisty of 5-HT, RF-amide and SCPV.Histochemistry 91:123–131.PubMedGoogle Scholar
  58. Reuter, M., Karhi, T., and Schot, L. P. C. (1984). Immunocytochemical demonstration of peptidergic neurons in the central and peripheral nervous system of the flatwormMicrostomum lineare with antiserum to FMRF-amide.Cell Tissue Res. 238:431–436.PubMedGoogle Scholar
  59. Reuter, M., Wikgren, M., and Lehtonen M. (1986). Immunocytochemical demonstration of 5-HT-like and FMRF-amide-like substances in whole mounts ofMicrostomum lineare (Turbellaria).Cell Tissue Res. 246:7–12.Google Scholar
  60. Reuter, M., Maule, A. G., Halton, D. W., Gustafsson, M. K. S., and Shaw, C. (1995). The organization of the nervous system in Plathelminthes. The neuropeptide F (NPF)-immunoreactive pattern in Catenulida, Macrostomida and Proseriata.Zoomorphology 115:83–97.Google Scholar
  61. Rieger, M. R. (1986) Asexual reproduction and the turbellarian archetype.Hydrobiologia 132:35–45.Google Scholar
  62. Saló, E. and Baguñà, J. (1986). Stimulation of cellular proliferation and differentiation in the intact and regenerating planarianDugesia (G) tigrina by the neuropeptide substance P.J. Exp. Zool. 237:129–135.PubMedGoogle Scholar
  63. Skuce, P. J., Johnston, C. F., Fairweather, I., Halton, D. W., and Shaw, C. (1990). A confocal scanning laser microscope study of the peptidergic and serotoninergic components of the nervous system in larvalSchistosoma mansoni, Parasitology 101:227–234.PubMedGoogle Scholar
  64. Steele, V. E., and Lange, C. S. (1977). Characterization of an organ-pecific differentiator substance in the planarianDugesia etrusca.J. Embryol. Exp. Morphol. 37:159–172.PubMedGoogle Scholar
  65. Sukhdeo, S. C., and Sukhdeo, M. V. K. (1994). FMRFamide-related peptides inHymenolepis diminuta: Immunocytochemistry and radioimmunoassay.Parasitol. Res. 80:374–380.PubMedGoogle Scholar
  66. Webb, R. A. (1988). Endocrinology of Acoelomates. In (H. Laufer and R. G. H. Downer, Eds.),Endocrinology of Selected Invertebrate Types, Alan R. Liss, New York, pp. 31–62.Google Scholar
  67. Westermann, R., Grothe, C., and Unsicker, K. (1990). Basic fibroblast growth factor (bFGF), a multifunctional growth factor for neuroectodermal cellsJ. Cell Sci. Suppl. 13:97–117.PubMedGoogle Scholar
  68. Wikgren, M. C. (1986). The nervous system of early larval stages of the cestodeDiphyllobothrium dendriticum.Acta Zool. (Stockh.) 67:155–163.Google Scholar
  69. Wikgren, B.-J. P., and Gustafsson, M. K. S. (1971). Cell proliferation and histogensis in Diphyllobothriid tapeworms (Cestoda).Acta Acad. Aboensis B 31(2):1–10.Google Scholar
  70. Wikgren, B.-J. P., and Knuts, G. M. (1970). Growth of the tegumental tissue in cestodes by cell migration.Acta Acad. Aboensis V 30:1–6.Google Scholar
  71. Wikgren, M. C., and Thorndyke, M. C. (1990). An echinoderm neuropeptide in flatworms?Acta Acad. Aboensis Ser. B 50(7):45–52.Google Scholar
  72. Wikgren, B.-J. P., Gustafsson, M. K. S., and Knuts, G. M. (1971). Primary anlage formation in Diphyllobothriid tapeworms.Z. Parasitenk. 36:131–139.Google Scholar
  73. Wikgren, M., Reuter, M., Gustafsson, M. K. S., and Lindroos, P. (1990). Immunocytochemical localization of histamine in flatworms.Cell Tissue Res. 260:479–484.PubMedGoogle Scholar
  74. Yoshizawa, Y., Wakabayashi, K., and Shinozawa, T. (1991). Inhibition of planarian regeneration by melatonin.hydrobiologia 227:31–40.Google Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • Maria Reuter
    • 1
  • Margaretha Gustafsson
    • 1
  1. 1.Department of BiologyÅbo Akademi University, BioCityÅboFinland

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