Skip to main content

Advertisement

Log in

Effects of neuropeptide F on regeneration in Girardia tigrina (Platyhelminthes)

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The effects of neuropeptide F (NPF; from Moniezia expansa) on the regeneration of Girardia tigrina were studied. The animals were decapitated and incubated in water (control) or NPF. The dynamics of the proliferation of the neoblasts in the developing tissue were studied during the course of regeneration by monitoring the mitotic index (MI). The effects of incubation in FMRFamide and GYIRFamide on the MI were also tested. The course of cephalic regeneration was followed with in vivo computer-assisted morphometry for up to 7 days. The development of the regenerating nervous system and the musculature was visualised by immunostaining with a primary antiserum to the C-terminal decapeptide of NPF (YFAIIGRPRFa) and tetramethylrhodamine-isothiocyanate-conjugated phalloidin, which stains F-actin in muscle filaments. The study showed that NPF had a stimulatory effect on the mitotic activity of the neoblasts. FMRFamide and GYIRFamide did not have this effect. NPF also stimulated the growth of the regenerating head and the growing nervous system and musculature. NPF is postulated to have a morphogenetic action in the regenerating animals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baguñà J (1974) Dramatic mitotic response in planarian after feeding, and a hypothesis for the control mechanism. J Exp Zool 190:117–122

    Article  PubMed  Google Scholar 

  • Baguñà J (1976a) Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. I. Mitotic studies during growth, feeding and starvation. J Exp Zool 195:53–64

    Article  Google Scholar 

  • Baguñà J (1976b) Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. II. Mitotic studies during regeneration, and a possible mechanism of blastema formation. J Exp Zool 195:65–80

    Article  Google Scholar 

  • Baguñà J (1981) Planarian neoblasts. Nature 290:14–15

    Article  Google Scholar 

  • Baguñà J, Romero R (1981) Quantitative analysis of cell types during growth, degrowth and regeneration in the planarians Dugesia mediterranea and Dugesia tigrina. Hydrobiologia 84:181–194

    Article  Google Scholar 

  • Baguñà J, Saló E, 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

    PubMed  Google Scholar 

  • Bode A, Salvenmoser W, Nimeth K, Mahlknecht M, Adamski Z, Rieger RM, Peter, R, Ladurner P (2006) Immunogold-labeled S-phase neoblasts, total neoblast number, their distribution, and evidence for arrested neoblasts in Macrostomum ligano (Platyhelminthes, Rhabditophora). Cell Tissue Res 325:577–587

    Article  PubMed  CAS  Google Scholar 

  • Brain SD, Cox HM (2006) Neuropeptides and their receptors. Br J Pharmacol 147:S202–S211

    Article  PubMed  CAS  Google Scholar 

  • Brown MR, Crim JW, Arata RC, Cai HN, Chun C, Shen P (1999) Identification of a Drosophila brain-gut peptide related to neuropeptide Y family. Peptides 20:1035–1042

    Article  PubMed  CAS  Google Scholar 

  • Cerstiaens A, Benfekih L, Zouiten H, Verhaert P, De Loof A, Schoof L (1999) Led-NPF-1 stimulates ovarian development in locusts. Peptides 20:39–44

    Article  PubMed  CAS  Google Scholar 

  • Coons AH, Leduc EH, Conolly JM (1955) Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J Exp Med 120:49–60

    Article  Google Scholar 

  • Curry WJ, Shaw C, Johnston CF, Thim L, Buchanan KD (1992) Neuropeptide F: primary structure from turbellarian, Artioposthia triangulata. Comp Biochem Physiol [C] Pharmacol Toxicol Endocrinol 101:269–274

    Article  CAS  Google Scholar 

  • Day TA, Maule AG (1999) Parasitic peptides! The structure and function of neuropeptides in parasitic worms. Peptides 20:999–1019

    Article  PubMed  CAS  Google Scholar 

  • de Jong-Brink M, Maat A, Tensen CP (2001) NPY in invertebrates: molecular answers to altered functions during evolution. Peptides 22:309–315

    Article  PubMed  Google Scholar 

  • Dougan PM, Mair GR, Halton DW, Curry WJ, Day TA, Maule AG (2002) Gene organization and expression of a neuropeptide Y homolog from the land planarian Arthurdendyus triangulatus. J Comp Neurol 454:58–64

    Article  PubMed  CAS  Google Scholar 

  • Friedl T, Webb RA (1979) Stimulation of mitoses in Dugesia tigrina by a neurosecretory fraction. Can J Zool 57:1818–1819

    Google Scholar 

  • Garczynski S, Crim JW, Brown MR (2005) Characterization of neuropeptide F and its receptor from African malaria mosquito, Anophelis gambiae. Peptides 26:99–107

    Article  PubMed  CAS  Google Scholar 

  • Gschwentner R, Ladurner P, Nimeth K, Rieger RM (2001) Stem cells in a basal bilaterian: S-phase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell Tissue Res 304:401–408

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson MKS (1976) Observations on the histogenesis of nervous tissue in Diphyllobothrium dendriticum Nitsch, 1824 (Cestoda, Pseudophyllidea). Z Parasitenk 50:313–321

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson MKS, Halton DW (2001) Nervous system of Platyhelminthes. In: Mehlhorn H (ed) Encyclopedic references of parasitology: biology, structure, function. Springer, Berlin Heidelberg New York, pp 423–439

    Google Scholar 

  • Gustafsson MKS, Halton DW, Kreshchenko ND, Movsessian SO, Raikova OI, Reuter M, Terenina NB (2002) Neuropeptides in flatworms. Peptides 23:2053–2061

    Article  PubMed  CAS  Google Scholar 

  • Halton DW, Maule AG (2004) Flatworm nerve-muscle: structural and functional analysis. Can J Zool 82:316–333

    Article  Google Scholar 

  • Hansel DE, Elpper BA, Ronnett GV (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410:940–944

    Article  PubMed  CAS  Google Scholar 

  • Hori I (1997) Cytological approach to morphogenesis in the planarian blastema. II. The effect of neuropeptides. J Submicrosc Cytol Pathol 29:91–97

    PubMed  CAS  Google Scholar 

  • Hori I, Kishida Y (2003) Quantitative changes in nuclear pores and chromatoid bodies induced by neuropeptides during differentiation in the planarian Dugesia japonica. J Submicrosc Cytol Pathol 35:439–444

    PubMed  CAS  Google Scholar 

  • Hrchková G, Velebný S, Halton DW, Day TA, Maule AG (2004) Pharmacological characterization of neuropeptide F (NPF)-induced effects on the motility of Mesocestoides corti (syn. Mesocestoides vogae) larvae. Int J Parasitol 34:83–93

    Article  CAS  Google Scholar 

  • Humphries JE, Kimber MJ, Barton Y-W, Hsu W, Marks NJ, Greer B, Harriot P, Maule AG, Day T (2004) Structure and bioactivity of neuropeptide F from the human parasites Schistosoma mansoni and Schistosoma japonicum. J Biol Chem 279:39880–39885

    Article  PubMed  CAS  Google Scholar 

  • Huybrechts J, De Loof A, Schoofs L (2004) Diapausing Colorado potato beetle are devoid of the short neuropeptide F I and II. Biochem Biophys Res Commun 317:909–916

    Article  PubMed  CAS  Google Scholar 

  • Kreshchenko ND, Reuter M, Sheiman, IM, Halton DW, Maule AG, Johnston RN, Shaw C, Gustafsson MKS (1999) Relationship between musculature and nervous system in the regenerating pharynx in Girardia tigrina (Plathelminthes). Invert Reprod Dev 35:109–125

    Google Scholar 

  • Kreshchenko N, Sheiman I, Reuter M, Gustafsson MKS, Halton DW, Maule AG (2001) Effects of FMRFamide-related peptides and neuropeptide F on planarian regeneration (Platyhelminthes, Tricladida). Belg J Zool 131(S1):147–148

    Google Scholar 

  • Ladurner P, Rieger RM, Baguñà J (2000) 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

    Article  PubMed  CAS  Google Scholar 

  • Mair GR, Halton DW, Shaw C, Maule AG (2000) The neuropeptide F (NPF) encoding gene from the cestode, Moniezia expansa. Parasitology 120:71–77

    Article  PubMed  CAS  Google Scholar 

  • Mair GR, Niciu MJ, Stewart MT, Brennan G, Omar H, Halton DW, Mains R, Eipper BA, Maule AG, Day TA (2004) A functionally atypical amidating enzyme from the human parasite Schistosoma mansoni. FASEB J 18:114–121

    Article  PubMed  CAS  Google Scholar 

  • Marks NJ, Johnson S, Halton DW, Shaw C, Geary TG, Moore S, et al (1996) Physiological effects of platyhelminth RFamide peptides on muscle strip preparations of Fasciola hepatica (Trematoda, Digenea). Parasitology 113:394–401

    Article  Google Scholar 

  • Maule AG, Shaw C, Halton DW, Thim L, Johnston CF, Fairweather I, Buchanan KD (1991) Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda:Cyclophyllidea). Parasitology 102:309–316

    CAS  Google Scholar 

  • McVeigh P, Kimber MJ, Novozhilova E, Day TA (2005) Neuropeptide signaling system in flatworms. Parasitology 131:S41–S55

    Article  PubMed  CAS  Google Scholar 

  • Morita M, Best JB (1984) Electron microscopic studies of planarian regeneration. IV. Cell division of neoblasts in Dugesia dorotocephala. J Exp Zool 229:425–436

    Article  Google Scholar 

  • Newmark PA, Sanchez Alvarado A (2000) Bromodeoxyuridine specially labels the regenerative stem cells of planarians. Dev Biol 220:142–153

    Article  PubMed  CAS  Google Scholar 

  • Nie M, Selbie LA (1998) Neuropeptide Y Y1 and Y2 receptor-mediated stimulation of mitogen-activated protein kinase activity. Regul Pept 75–76:207–213

    Article  Google Scholar 

  • Nimeth KT, Mahlknecht M, Mezzanato A, Peter R, Rieger R, Ladurner P (2004) Stem cell dynamics during growth, feeding, and starvation in the basal flatworm Microstomum sp. (Platyhelminthes). Dev Dyn 230:91–99

    Article  PubMed  Google Scholar 

  • Nimeth KT, Egger B, Rieger R, Salvenmoser W, Peter R, Gschwentner R (2007) Regeneration in Macrostomum ligano (Platyhelminthes): cellular dynamics in the neoblast stem cell system. Cell Tissue Res 327:637–646

    Article  PubMed  CAS  Google Scholar 

  • Orii H, Sakurai T, Watanabe K (2005) Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev Gen Evol 215:145–157

    Article  CAS  Google Scholar 

  • Pedrazzini T (2004) Importance of NPY Y1 receptor-mediated pathways: assessment using NPY Y1 receptor knockouts. Neuropeptides 38:267–275

    Article  PubMed  CAS  Google Scholar 

  • Rajpara SM, Garcia PD, Roberts R, Eliassen JC, Owens DF, Maltby D, Myers RM, Mayeri E (1992) Identification and molecular cloning of neuropeptide Y homolog that produces prolonged inhibition in Aplysia neurons. Neuron 9:505–513

    Article  PubMed  CAS  Google Scholar 

  • Reddien PW, Sanchez Alvarado A (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20:725–757

    Article  PubMed  CAS  Google Scholar 

  • Reuter M, Halton DW (2001) Comparative neurobiology of Platyhelminthes. In: Littlewood TJ, Bray RA (eds) The interelationships of platyhelminthes. Academic Press, London, pp 239–259

    Google Scholar 

  • Reuter M, Kreshchenko N (2004) Flatworm asexual multiplication implicates stem cells and regeneration. Can J Zool 82:334–356

    Article  Google Scholar 

  • Reuter M, Gustafsson MKS, Sheiman IM, Terenina N, Halton DW, Maule AG, Shaw C (1995) The nervous system of Tricladida. II. Neuroanatomy of Dugesia tigrina (Plaudicola, Dugesiidae): an immunocytochemical study. Invert Neurosci 1:133–143

    Article  PubMed  CAS  Google Scholar 

  • Reuter M, Sheiman IM, Gustafsson MKS, Halton DW, Maule AG, Shaw C (1996) Development of the nervous system in Dugesia tigrina during regeneration after fission and decapitation. Invert Reprod Dev 29:199–211

    Google Scholar 

  • Saló E (2006) The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). BioEssays 28:546–559

    Article  PubMed  CAS  Google Scholar 

  • Saló E, Baguñà J (1984) 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

    PubMed  Google Scholar 

  • Saló E, Baguñà J (1985) Cell movement in intact and regenerating planarians. Quantitation using chromosomal nuclear and cytoplasmic markers. J Embryol Exp Morphol 89:57–79

    PubMed  Google Scholar 

  • Saló E, Baguñà J (1989) Regeneration and pattern formation in planarians. II. Local origin and role of cell movements in blastema formation. Development 107:69–76

    Google Scholar 

  • Saló E, Baguñà J (2002) Regeneration in planarians and other worms: new findings, new tools, and new perspectives. J Exp Zool 292:528–539

    Article  PubMed  Google Scholar 

  • Sanchez Alvarado A (2006) Planarian regeneration: its end is its beginning. Cell 124:241–245

    Article  PubMed  CAS  Google Scholar 

  • Sauzin-Monnot MJ (1975) Étude ultrastructural de la régénération chez Dugesia gonocephala et Polycelis nigra, planaires á pouvoir de régénération totale, et chez Dendrocoelum lacteum, planaire á pouvoir de régénération céphalique limitée (Turbellarié, Tricladides). Bull Soc Zool Fr 100:293–304

    Google Scholar 

  • Sheiman IM, Tiras KhP, Balobanova EF (1989) The morphogenetic effects of neuropeptides. Fiziologicheskii Zhurnal SSSR (Physiological Journal) 75:619–626

    CAS  Google Scholar 

  • Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y—a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660

    Article  PubMed  CAS  Google Scholar 

  • Tiras KP, Rubina AU, Miloserdov YV, Tishchenko VA (1990) Hydra morphogen as possible endogenous stimulator of planarian regeneration. In: Sheiman IM (ed) Morphogenetically active substances. Academy of Science USSR, Pushchino, pp 134–145

    Google Scholar 

  • Wolpert L, Beddington R, Brockers J, Jessell T, Lawrence P, Meyerowitz E (1999) Entwicklungsbiologie. Spectrum Akademischer, Heidelberg Berlin

    Google Scholar 

Download references

Acknowledgements

We are grateful for the constructive comments of the referees.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Margaretha K. S. Gustafsson.

Additional information

This work was supported by two grants from the Finnish Academy of Science (nos. 202685, 2004) and (no. 112090, 2006) to M.G., an RFBR grant (07-04-00452a) to N.K. and a Wellcome Trust grant (069411) to A.G.M. for which we express our gratitude.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kreshchenko, N.D., Sedelnikov, Z., Sheiman, I.M. et al. Effects of neuropeptide F on regeneration in Girardia tigrina (Platyhelminthes). Cell Tissue Res 331, 739–750 (2008). https://doi.org/10.1007/s00441-007-0519-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-007-0519-y

Keywords

Navigation