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Echinococcus multilocularis as an experimental model in stem cell research and molecular host-parasite interaction

Published online by Cambridge University Press:  07 December 2009

K. BREHM
K. BREHM*
Affiliation:
University of Würzburg, Institute of Hygiene and Microbiology, Josef-Schneider-Strasse 2, D-97080Würzburg, Germany
*
*Corresponding author: Institute of Hygiene and Microbiology, University of Würzburg, Josef-Schneider-Strasse 2, D-97080Würzburg, Germany. Tel: +49 931 201 46168. Fax: +49 931 201 46445. E-mail: [email protected]
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Summary

Totipotent somatic stem cells (neoblasts) are key players in the biology of flatworms and account for their amazing regenerative capability and developmental plasticity. During recent years, considerable progress has been made in elucidating molecular features of neoblasts from free-living flatworms, whereas their role in parasitic species has so far merely been addressed by descriptive studies. Very recently, however, significant advances have been made in the in vitro culture of neoblasts from the cestode Echinococcus multilocularis. The isolated cells proved capable of generating mature metacestode vesicles under laboratory conditions in a manner that closely resembles the oncosphere-metacestode transition during natural infections. Using the established neoblast cultivation protocols, combined with targeted manipulation of Echinococcus genes by RNA-interference, several fundamental questions of host-dependent parasite development can now be addressed. Here, I give an overview of current cultivation techniques for E. multilocularis neoblasts and present experimental approaches to study their function. Furthermore, I introduce the E. multilocularis genome sequencing project that is presently in an advanced stage. The combined input of data from the E. multilocularis sequencing project, stem cell cultivation, and recently initiated attempts to genetically manipulate Echinococcus will provide an ideal platform for hypothesis-driven research into cestode development in the next years.

Keywords

Echinococcuscestodeparasitegenomeregenerationneoblaststem cellantigen Bhost-parasite interactionin vitro cultivation
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 537 - 555
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Ali-Khan, Z., Siboo, R., Gomersall, M. and Faucher, M. (1983). Cystolytic events and the possible role of germinal cells in metastasis in chronic alveolar hydatidosis. Annals of Tropical Medicine and Parasitology 77, 497–512.CrossRefGoogle ScholarPubMed
Amikura, R., Hanyu, K., Kashikawa, M. and Kobayashi, S. (2001 a). Tudor protein is essential for the localization of mitochondrial RNAs in polar granules of Drosophila embryos. Mechanisms of Development 107, 97–104.CrossRefGoogle ScholarPubMed
Amikura, R., Kashikawa, M., Nakamura, A. and Kobayashi, S. (2001 b). Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proceedings of the National Academy of Sciences, USA 98, 9133–9138.CrossRefGoogle ScholarPubMed
Amikura, R., Sato, K. and Kobayashi, S. (2005). Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mechanisms of Development 122, 1087–1093.CrossRefGoogle ScholarPubMed
Arend, A. C., Zaha, A., Ayala, F. J. and Haag, K. L. (2004). The Echinococcus granulosus antigen B shows a high degree of genetic variability. Experimental Parasitology 108, 76–80.CrossRefGoogle Scholar
Babitt, J. L., Huang, F. W., Xia, Y., Siodis, Y., Andrews, N. C. and Lin, H. Y. (2007). Modulation of bone morphogenetic protein signalling in vivo regulates systemic iron balance. Journal of Clinical Investigation 117, 1933–1939.CrossRefGoogle ScholarPubMed
Beall, M. J. and Pearce, E. J. (2001). Human transforming growth factor-β activates a receptor serine/threonin kinase from the intravascular parasite Schistosoma mansoni. Journal of Biological Chemistry 276, 31613–31619.CrossRefGoogle ScholarPubMed
Botero, D. (1970). Paromomycin as effective treatment of Taenia infections. American Journal of Tropical Medicine and Hygiene 19, 234–237.CrossRefGoogle ScholarPubMed
Brehm, K., Hubert, K., Sciutto, E., Garate, T. and Frosch, M. (2002). Characterization of a spliced leader gene and of trans-spliced mRNAs from Taenia solium. Molecular and Biochemical Parasitology 122, 105–110.CrossRefGoogle ScholarPubMed
Brehm, K., Jensen, K. and Frosch, M. (2000 a). mRNA trans-splicing in the human parasitic cestode Echinococcus multilocularis. Journal of Biological Chemistry 275, 38311–38318.CrossRefGoogle ScholarPubMed
Brehm, K., Kronthaler, K., Jura, H. and Frosch, M. (2000 b). Cloning and characterization of β-tubulin genes from Echinococcus multilocularis. Molecular and Biochemical Parasitology 107, 297–302.CrossRefGoogle ScholarPubMed
Brehm, K. and Spiliotis, M. (2008 a). Recent advances in the in vitro cultivation and genetic manipulation of Echinococcus multilocularis metacestodes and germinal cells. Experimental Parasitology 119, 506–515.CrossRefGoogle ScholarPubMed
Brehm, K. and Spiliotis, M. (2008 b). The influence of host hormones and cytokines on Echinococcus multilocularis signalling and development. Parasite 15, 286–290.CrossRefGoogle ScholarPubMed
Brehm, K., Spiliotis, M., Zavala-Góngora, R., Konrad, C. and Frosch, M. (2006). The molecular mechanisms of larval cestode development: first steps into an unknown world. Parasitology International 55, S15–S21.CrossRefGoogle ScholarPubMed
Brehm, K., Wolf, M., Beland, H., Kroner, A. and Frosch, M. (2003). Analysis of differential gene expression in Echinococcus multilocularis larval stages by means of spliced leader differential display. International Journal for Parasitology 33, 1145–1159.CrossRefGoogle ScholarPubMed
Buttarelli, F. R., Pellicano, C. and Pontieri, F. E. (2008) Neuropharmacology and behaviour in planarians: translation to mammals. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 147, 399–408.Google ScholarPubMed
Cheng, G., Cohen, L., Mikhli, C., Jankowska-Anyszka, M., Stepinski, J., Darzynkiewicz, E. and Davis, R. E. (2007). In vivo translation and stability of trans-spliced mRNAs in nematode embryos. Molecular and Biochemical Parasitology 153, 95–106.CrossRefGoogle ScholarPubMed
Cheng, G., Cohen, L., Ndegwa, D. and Davis, R. E. (2006). The flatworm spliced leader 3′-terminal AUG as a translation initiator methionine. Journal of Biological Chemistry 281, 733–743.CrossRefGoogle Scholar
Chow, C., Gauci, C. G., Cowman, A. F. and Lightowlers, M. W. (2001). A gene family expressing a host-protective antigen of Echinococcus granulosus. Molecular and Biochemical Parasitology 118, 83–88.CrossRefGoogle ScholarPubMed
Coustau, C. and Yoshino, T. P. (2000) Flukes without snails: advances in the in vitro cultivation of intramolluscan stages of trematodes. Experimental Parasitology 94, 62–66.CrossRefGoogle ScholarPubMed
Davis, R. E., Hardwick, C., Tavernier, P., Hodgson, S. and Singh, H. (1995). RNA trans-splicing in flatworms. Analysis of trans-spliced mRNAs and genes in the human parasite, Schistosoma mansoni. Journal of Biological Chemistry 270, 21813–21819.CrossRefGoogle ScholarPubMed
Davis, R. E., Singh, H., Botka, C., Hardwick, C., Ashraf el Meanawy, M. and Villanueva, J. (1994). RNA trans-splicing in Fasciola hepatica. Identification of a spliced leader (SL) RNA and SL sequences on mRNAs. Journal of Biological Chemistry 269, 20026–20030.CrossRefGoogle ScholarPubMed
Delcuve, G. P., Rastegar, M. and Davie, J. R. (2009). Epigenetic control. Journal of Cellular Physiology 219, 243–250.CrossRefGoogle ScholarPubMed
Dowling, R. J., Pollak, M. and Sonenberg, N. (2009). Current status and challenges associated with targeting mTOR for cancer therapy. BioDrugs 23, 77–91.CrossRefGoogle ScholarPubMed
Drummond-Barbosa, D. (2008). Stem cells, their niches and the systemic environment: an aging network. Genetics 180, 1787–1797.CrossRefGoogle ScholarPubMed
Eisenhoffer, G. T., Kang, H. and Sanchez-Alvarado, A. (2008). Molecular analysis of stem cells and their descendents during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 11, 327–339.CrossRefGoogle Scholar
Fausto, N. (2000). Liver regeneration. Journal of Hepatology 32, 19–31.CrossRefGoogle ScholarPubMed
Fernandez, C., Gregory, W. F., Loke, P. and Maizels, R. M. (2002). Full-length cDNA libraries from Echinococcus granulosus contain separate populations of oligo-capped and trans-spliced transcripts and a high level of predicted signal peptide sequences. Molecular and Biochemical Parasitology 122, 171–180.CrossRefGoogle Scholar
Galindo, M., Paredes, R., Marchant, C., Mino, V. and Galanti, N. (2003). Regionalization of DNA and protein synthesis in developing stages of the parasitic platyhelminth Echinococcus granulosus. Journal of Cellular Biochemistry 90, 294–303.CrossRefGoogle ScholarPubMed
Gan, Q., Yoshida, T., McDonald, O. G. and Owens, G. K. (2007). Epigenetic mechanisms contribute to pluripotency and cell lineage determination of embryonic stem cells. Stem Cells 25, 2–9.CrossRefGoogle ScholarPubMed
Gangaraju, V. K. and Lin, H. (2009). MicroRNAs: key regulators of stem cells. Nature Reviews Molecular Cell Biology 10, 116–125.CrossRefGoogle ScholarPubMed
Gelmedin, V., Caballero-Gamiz, R. and Brehm, K. (2008). Characterization and inhibition of a p38-like mitogen-activated protein kinase (MAPK) from Echinococcus multilocularis: antiparasitic activities of p38 MAPK inhibitors. Biochemical Pharmacology 76, 1068–1081.CrossRefGoogle ScholarPubMed
Gelmedin, V., Spiliotis, M. and Brehm, K. (2009). Molecular characterisation of MEK1/2- and MKK3/6-like mitogen-activated protein kinase kinases (MAPKK) from the fox-tapeworm Echinococcus multilocularis. International Journal for Parasitology, in press, doi:10.1016/j.ijpara.2009.10.009Google Scholar
Gelmedin, V., Zavala-Gongora, R., Fernandez, C. and Brehm, K. (2005). Echinococcus multilocularis: cloning and characterization of a member of the SNW/SKIP family of transcriptional coregulators. Experimental Parasitology 111, 115–120.CrossRefGoogle ScholarPubMed
Gilleard, J. S. (2004). The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 128, S49–S70.Google Scholar
Gomez-Escobar, N., Gregory, W. F. and Maizels, R. M. (2000). Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor-β, expressed in microfilarial and adult stages of Brugia malayi. Infection and Immunity 68, 6402–6410.CrossRefGoogle ScholarPubMed
Guo, T., Peters, A. H. F. M. and Newmark, P. A. (2006). A bruno-like gene is required for stem cell maintenance in planarians. Developmental Cell 11, 159–169.CrossRefGoogle ScholarPubMed
Guo, X. and Wang, X. F. (2009). Signaling cross-talk between TGF-β/BMP and other pathways. Cell Research 19, 71–88.CrossRefGoogle ScholarPubMed
Gur, Y. and Breitbart, H. (2008). Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Molecular and Cellular Endocrinology 282, 45–55.CrossRefGoogle ScholarPubMed
Haag, K. L., Alves-Junior, L., Zaha, A. and Ayala, F. J. (2004). Contingent, non-neutral evolution in a multicellular parasite: natural selection and gene conversion in the Echinococcus granulosus antigen B gene family. Gene 333, 157–167.CrossRefGoogle Scholar
Hamilton, T. L., Stoneley, M., Spriggs, K. A. and Bushell, M. (2006). TOPs and their regulation. Biochemical Society Transactions 34, 12–16.CrossRefGoogle ScholarPubMed
Harraga, S., Godot, V., Bresson-Hadni, S., Mantion, G. and Vuitton, D. A. (2003). Profile of cytokine production within the periparasitic granuloma in human alveolar echinococcosis. Acta Tropica 85, 231–236.CrossRefGoogle ScholarPubMed
Harris, A., Heath, D. D., Lawrence, S. B. and Shaw, R. J. (1989). Echinococcus granulosus: ultrastructure of epithelial changes during the first 8 days of metacestode development in vitro. International Journal for Parasitology 19, 621–629.CrossRefGoogle ScholarPubMed
Heath, D. D. and Lawrence, S. B. (1976). Echinococcus granulosus: development in vitro from oncosphere to immature hydatid cyst. Parasitology 73, 417–423.CrossRefGoogle ScholarPubMed
Hemphill, A. and Gottstein, B. (1995). Immunology and morphology studies on the proliferation of in vitro cultivated Echinococcus multilcoularis metacestodes. Parasitology Research 81, 605–614.CrossRefGoogle Scholar
Higuchi, S., Hayashi, T., Hori, I., Shibata, N., Sakamoto, H. and Agata, K. (2007). Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis. Development, Growth and Differentiation 49, 571–581.CrossRefGoogle Scholar
Hori, I. (1982). An ultrastructural study of the chromatoid body in planarian regenerative cells. Journal of Electron Microscopy 31, 63–72.Google Scholar
Ito, H., Saito, Y., Watanabe, K. and Orii, H. (2001). Epimorphic regeneration of the distal part of the planarian pharynx. Developmental Genes and Evolution 211, 2–9.CrossRefGoogle ScholarPubMed
Jastrzebski, K., Hannan, K. M., Tchoubrieva, E. B., Hannan, R. D. and Pearson, R. B. (2007). Coordinate regulation of ribosome biogenesis and function by the ribosomal protein S6 kinase, a key mediator of mTOR function. Growth Factors 25, 209–226.CrossRefGoogle ScholarPubMed
Jura, H., Bader, A., Hartmann, M., Maschek, H. and Frosch, M. (1996). Hepatic tissue culture model for study of host-parasite interactions in alveolar echinococcosis. Infection and Immunity 64, 3484–3490.CrossRefGoogle ScholarPubMed
Kaiser, P., Rothwell, L., Avery, S. and Balu, S. (2004). Evolution of the interleukins. Developmental and Comparative Immunology 28, 374–394.CrossRefGoogle ScholarPubMed
Kashikawa, M., Amikura, R. and Kobayashi, S. (2001). Mitochondrial small ribosomal RNA in a component of germinal granules in Xenopus embryos. Mechanisms of Development 101, 71–77.CrossRefGoogle Scholar
Khayath, N., Vicogne, J., Ahier, A., BenYounes, A., Konrad, C., Trolet, J., Viscogliosi, F., Brehm, K. and Dissous, C. (2007). Diversification of the insulin receptor family in the helminth parasite Schistosoma mansoni. FEBS Journal 274, 659–676.CrossRefGoogle ScholarPubMed
Kines, K. J., Morales, M. E., Mann, V. H., Gobert, G. N. and Brindley, P. J. (2008). Integration of reporter transgenes into Schistosoma mansoni chromosomes mediated by pseudotyped murine leukemia virus. FASEB Journal 22, 2936–2948.CrossRefGoogle ScholarPubMed
Kinoshita, K., Iimuro, Y., Otogawa, K., Saika, S., Inagaki, Y., Nakajima, Y., Kawada, N., Fujimoto, J., Friedman, S. L. and Ikeda, K. (2007). Adenovirus-mediated expression of BMP-7 suppresses the development of liver fibrosis in rats. Gut 56, 706–714.CrossRefGoogle ScholarPubMed
Kobayashi, S., Sato, K. and Hayashi, Y. (2005). The role of mitochondrial rRNAs and Nanos protein in germline formation in Drosophila embryos. Zoological Science 22, 943–954.CrossRefGoogle ScholarPubMed
Konrad, C., Kroner, A., Spiliotis, M., Zavala-Gongora, R. and Brehm, K. (2003). Identification and molecular characterization of a gene encoding a member of the insulin receptor family in Echinococcus multilocularis. International Journal for Parasitology 33, 301–312.CrossRefGoogle ScholarPubMed
Kotaja, N. and Sassone-Corsi, P. (2007). The chromatoid body: a germ-cell-specific RNA-processing centre. Nature Reviews Molecular Cell Biology 8, 85–90.CrossRefGoogle ScholarPubMed
Lall, S., Friedman, C. C., Jankowska-Anyszka, M., Stepinski, J., Darzynkiewicz, E. and Davis, R. E. (2004). Contribution of trans-splicing, 5′-leader length, cap-poly(A) synergism, and initiation factors to nematode translation in an Ascaris suum embryo cell-free system. Journal of Biological Chemistry 279, 45573–45585.CrossRefGoogle Scholar
Lau, A. H., Knakievicz, T., Prá, D. and Erdtmann, B. (2007). Freshwater planarians as novel organisms for genotoxicity testing: analysis of chromosome aberrations. Environmental and Molecular Mutagenesis 48, 475–482.CrossRefGoogle ScholarPubMed
Long, X., Müller, F. and Avruch, J. (2004). TOR action in mammalian cells and in Caenorhabditis elegans. Current Topics in Microbiology and Immunology 279, 115–138.Google ScholarPubMed
Maki, J. and Yanagisawa, T. (1985). Anthelmintic effects of bithionol, paromomycin sulphate, flubendazole and mebendazole on mature and immature Hymenolepis nana in mice. Journal of Helminthology 59, 211–216.CrossRefGoogle ScholarPubMed
Mamane, Y., Petroulakis, E., Martineau, Y., Sato, T. A., Larsson, O., Rajasekhar, V. K. and Sonenberg, N. (2007). Epigenetic activation of a subset of mRNAs by eIF4E explains its effects on cell proliferation. PLoS ONE 2, e242.CrossRefGoogle ScholarPubMed
Mamuti, W., Sako, Y., Xiao, N., Nakaya, K., Nakao, M., Yamasaki, H., Lightowlers, M. W., Craig, P. S. and Ito, A. (2006). Echinococcus multilocularis: developmental stage-specific expression of Antigen B 8-kDa-subunits. Experimental Parasitology 113, 75–82.CrossRefGoogle ScholarPubMed
Mathis, A., Wild, P., Boettger, E. C., Kapel, C. M. O. and Deplazes, P. (2005). Mitochondrial ribosome as the target for the macrolide antibiotic clarithromycin in the helminth Echinococcus multilocularis. Antimicrobial Agents and Chemotherapy 49, 3251–3225.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Eckert, J. and Thompson, R. C. A. (1983). Proliferation and metastases formation of larval Echinococcus multilocularis. Zentralblatt für Parasitenkunde 69, 749–763.CrossRefGoogle ScholarPubMed
Mlocicki, D., Swiderski, Z., Miquel, J., Eira, C. and Conn, D. B. (2006). Cellular organization of the oncosphere of Mosgovoyia ctenoides (Cestoda: Anoplocephalidae). Journal of Parasitology 92, 953–961.CrossRefGoogle ScholarPubMed
Molina, M. D., Saló, E. and Cebrià, F. (2007). The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians. Developmental Biology 311, 79–94.CrossRefGoogle ScholarPubMed
Morris, D. L. and Taylor, D. H. (1990). Echinococcus granulosus: development of resistance to albendazole in an animal model. Journal of Helminthology 64, 171–174.Google Scholar
Morrison, S. J. and Spradling, A. C. (2008). Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132, 598–611.CrossRefGoogle ScholarPubMed
Nimeth, K. T., Mahlknecht, M., Mezzanato, A., Peter, R., Rieger, R. and Ladurner, P. (2004). Stem cell dynamics suring growth, feeding, and starvation in the basal flatworm Macrostomum sp. (Platyhelminthes). Developmental Dynamics 230, 91–99.CrossRefGoogle Scholar
Olson, P. D. (2008). Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitology International 57, 8–17.CrossRefGoogle ScholarPubMed
Oviedo, N. J. and Beane, W. S. (2009). Regeneration: The origin of cancer as a possible cure? Seminars in Cell and Developmental Biology 20, 557–564.CrossRefGoogle ScholarPubMed
Oviedo, N. J. and Levin, M. (2007). smedinx-11 is a planarian stem cell gap junction gene required for regeneration and homeostasis. Development 134, 3121–3131.Google Scholar
Oviedo, N. J., Pearson, B. J., Levin, M. and Sanchez-Alvarado, A. (2008). Planarian PTEN homologs regulate stem cells and regeneration through TOR signalling. Disease Models and Mechanisms 1, 131–143.CrossRefGoogle Scholar
Palakodeti, D., Smielewska, M., Lu, Y. C., Yeo, G. W. and Graveley, B. R. (2008). The PIWI proteins SMEDWI-1 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14, 1174–1186.CrossRefGoogle ScholarPubMed
Pearce, E. J. and Freitas, T. C. (2008). Reverse genetics and the study of the immune response to schistosomes. Parasite Immunology 30, 215–221.Google Scholar
Pearson, B. J. and Sanchez-Alvarado, A. (2008). Regeneration, stem cells, and the evolution of tumor suppression. Cold Spring Harbour Symposia on Quantitative Biology 73, 565–572.CrossRefGoogle ScholarPubMed
Rausch, R. (1954). Studies on the helminth fauna of Alaska. XX. The histogenesis of the alveolar larva of Echinococcus species. Journal of Infectious Diseases 94, 178–186.CrossRefGoogle ScholarPubMed
Reddien, P. W., Bermange, A. L., Murfitt, K. J., Jennings, J. R. and Sánchez-Alvarado, A. (2005). Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Developmental Cell 8, 635–649.Google Scholar
Reuter, M. and Kreshchenko, N. (2004). Flatworm asexual multiplication implicates stem cells and regeneration. Canadian Journal of Zoology 82, 334–356.CrossRefGoogle Scholar
Rieger, R. M., Legniti, A., Ladurner, P., Reiter, D., Asch, E., Salvenmoser, W., Schürmann, W. and Peter, R. (1999). Ultrastructure of neoblasts in microturbellaria: significance for understanding stem cells in free-living Platyhelminthes. Invertebrate Reproduction and Development 35, 127–140.CrossRefGoogle Scholar
Rossi, L., Salvetti, A., Batistoni, R., Deri, P. and Gremigni, V. (2008). Planarians, a tale of stem cells. Cellular and Molecular Life Sciences 65, 16–23.CrossRefGoogle ScholarPubMed
Rybicka, K. (1966). Embryogenesis in cestodes. Advances in Parasitology 4, 107–186.CrossRefGoogle ScholarPubMed
Sakamoto, T. (1981). Electron microscopical observations on the egg of Echinococcus multilocularis. Memoirs of the Faculty of Agriculture, Kagoshima University 17, 165–174.Google Scholar
Sakamoto, T. (1982). Histochemistry and histoenzymology of Echinococcus. I. Histochemical observation on general structure of Echinococcus multilocularis. Memoirs of the Faculty of Agriculture, Kagoshima University 18, 127–139.Google Scholar
Sakamoto, T. and Sugimura, M. (1970). Studies on Echinococcus XXIII. Electron microscopical observations on histogenesis of larval Echinococcus multilocularis. Japanese Journal of Veterinary Research 18, 131–144.Google Scholar
Saló, E. (2006). The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). BioEssays 28, 546–559.CrossRefGoogle ScholarPubMed
Saló, E., Abril, J. F., Adell, T., Cebriá, F., Eckelt, K., Fernandez-Taboada, E., Handberg-Thorsager, M., Iglesias, M., Dolores-Molina, M. and Rodriguesz-Esteban, G. (2009). Planarian regeneration: achievements and future directions after 20 years of research. International Journal of Developmental Biology 53, 1317–1327.CrossRefGoogle ScholarPubMed
Saló, E. and Baguna, J. (2002). Regeneration in planarians and other worms: new findings, new tools, and new perspectives. Journal of Experimental Zoology 292, 528–539.CrossRefGoogle ScholarPubMed
Salvetti, A., Rossi, L., Deri, P. and Batistoni, R. (2000). An MCM2-related gene is expressed in proliferating cells of intact and regenerating planarians. Developmental Dynamics 218, 603–614.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Salvetti, A., Rossi, L., Lena, A., Batistoni, R., Deri, P., Rainaldi, G., Locci, M. T., Evangelista, M. and Gremigni, V. (2005). DjPUM, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132, 1863–1874.CrossRefGoogle ScholarPubMed
Sanchez-Alvarado, A. (2006). Planarian regeneration: its end and its beginning. Cell 124, 241–245.CrossRefGoogle ScholarPubMed
Sanchez-Alvarado, A. and Kang, H. (2005). Multicellularity, stem cells, and the neoblast of the planarian Schmidtea mediterranea. Experimental Cell Research 306, 299–308.CrossRefGoogle ScholarPubMed
Sánchez-Alvarado, A. and Tsonis, P. A. (2006). Bridging the regeneration gap: genetic insights from diverse animal models. Nature Reviews Genetics 7, 873–884.CrossRefGoogle ScholarPubMed
Sato, K., Shibata, N., Orii, H., Amikura, R., Sakurai, T., Agata, K., Kobayashi, S. and Watanabe, K. (2006). Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Development, Growth and Differentiation 48, 615–628.CrossRefGoogle ScholarPubMed
Sato, K., Sugita, T., Kobayashi, K., Fujita, K., Fujii, T., Matsumoto, Y., Mikami, T., Nishizuka, N., Nishizuka, S., Shojima, K., Suda, M., Takahashi, G., Himeno, H., Muto, A. and Ishida, S. (2001). Localization of mitochondrial ribosomal RNA on the chromatoid bodies of marine polyclad embryos. Development, Growth and Differentiation 43, 107–114.CrossRefGoogle ScholarPubMed
Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature 441, 1075–1079.CrossRefGoogle ScholarPubMed
Schürmann, W. and Peter, R. (2001). Planarian cell culture: a comparative review of methods and an improved protocol for primary cultures of neoblasts. Belgian Journal of Zoology 131, 123–130.Google Scholar
Shibata, N., Umenoso, Y., Orii, H., Sakurai, T., Watanabe, K. and Agata, K. (1999). Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Developmental Biology 206, 73–87.CrossRefGoogle ScholarPubMed
Shojaee-Moradie, F., Powrie, J. K., Sundermann, E., Spring, M. W., Schüttler, A., Sönksen, P. H., Brandenburg, D. and Jones, R. H. (2000). Novel hepatoselective insulin analog: studies with a covalently linked thyroxyl-insulin complex in humans. Diabetes Care 23, 1124–1129.CrossRefGoogle ScholarPubMed
Siles-Lucas, M. and Hemphill, A. (2002). Cestode parasites: application of in vivo and in vitro models for studies on the host-parasite relationship. Advances in Parasitology 51, 133–230.CrossRefGoogle ScholarPubMed
Slais, J. (1973) Functional morphology of cestode larvae. Advances in Parasitology 11, 395–480.CrossRefGoogle ScholarPubMed
Solana, J., Lasko, P. and Romero, R. (2009). Spoltud-1 is a chromatoid body component required for planarian long-term stem cell self-renewal. Developmental Biology 328, 410–421.CrossRefGoogle ScholarPubMed
Spiliotis, M. and Brehm, K. (2004). Echinococcus multilocularis: identification and molecular characterization of a Ral-like small GTP-binding protein. Experimental Parasitology 107, 163–172.CrossRefGoogle ScholarPubMed
Spiliotis, M. and Brehm, K. (2009). Axenic in vitro cultivation of Echinococcus multilocularis metacestode vesicles and the generation of primary cell cultures. Methods in Molecular Biology 470, 245–262.CrossRefGoogle ScholarPubMed
Spiliotis, M., Konrad, C., Gelmedin, V., Tappe, D., Brückner, S., Mösch, H. U. and Brehm, K. (2006). Characterization of EmMPK1, an ERK-like MAP kinase from Echinococcus multilocularis which is activated in response to human epidermal growth factor. International Journal for Parasitology 36, 1097–1112.CrossRefGoogle ScholarPubMed
Spiliotis, M., Kroner, A. and Brehm, K. (2003). Identification, molecular characterization and expression of the gene encoding the epidermal growth factor receptor orthologue from the fox-tapeworm Echinococcus multilocularis. Gene 323, 57–65.CrossRefGoogle ScholarPubMed
Spiliotis, M., Lechner, S., Tappe, D., Scheller, C., Krohne, G. and Brehm, K. (2008). Transient transfection of Echinococcus multilocularis primary cells and complete in vitro regeneration of metacestode vesicles. International Journal for Parasitology 38, 1025–1039.CrossRefGoogle ScholarPubMed
Spiliotis, M., Tappe, D., Brückner, S., Mösch, H. U. and Brehm, K. (2005). Molecular cloning and characterization of Ras- and Raf-homologues from the fox-tapeworm Echinococcus multilocularis. Molecular and Biochemical Parasitology 139, 225–237.CrossRefGoogle ScholarPubMed
Spiliotis, M., Tappe, D., Sesterhenn, L. and Brehm, K. (2004). Long-term in vitro cultivation of Echinococcus multilocularis metacestodes under axenic conditions. Parasitology Research 92, 430–432.CrossRefGoogle ScholarPubMed
Standart, N. and Jackson, R. J. (2007). MicroRNAs repress translation of m7Gppp-capped target mRNAs in vitro by inhibiting initiation and promoting deadenylation. Genes and Development 21, 1975–82.CrossRefGoogle ScholarPubMed
Sugimoto, H., Yang, C., LeBleu, V. S., Soubasakos, M. A., Giraldo, M., Zeisberg, M. and Kalluri, R. (2007). BMP-7 functions as a novel hormone to facilitate liver regeneration. FASEB Journal 21, 256–264.CrossRefGoogle ScholarPubMed
Swiderski, Z. (1983) Echinococcus granulosus: hook-muscle systems and cellular organisation of infective oncospheres. International Journal for Parasitology 13, 289–299.CrossRefGoogle ScholarPubMed
Tanaka, E. M. and Weidinger, G. (2008). Heads or tails: can Wnt tell which one is up? Nature Cell Biology 10, 122–124.CrossRefGoogle ScholarPubMed
Tappe, D., Brehm, K., Frosch, M., Blankenburg, A., Schrod, A., Kaup, F. J. and Mätz-Rensing, K. (2007). Echinococcus multilocularis infection of several Old World monkey species in a breeding enclosure. American Journal of Tropical Medicine and Hygiene 77, 504–506.CrossRefGoogle Scholar
Truksa, J., Peng, H., Lee, P. and Beutler, E. (2007). Different regulatory elements are required for response of hepcidin to interleukin-6 and bone morphogenetic proteins 4 and 9. British Journal of Hepatology 139, 138–147.Google ScholarPubMed
Tysnes, B. B. and Bjerkvig, R. (2007). Cancer initiation and progression: involvement of stem cells and the microenvironment. Biochimica et Biophysica Acta 1775, 283–297.Google ScholarPubMed
van Staveren, W. C. G., Weiss-Solis, D. Y., Hebrant, A., Detours, V., Dumont, J. E. and Maenhaut, C. (2009). Human cancer cell lines: experimental models for cancer cells in situ? For cancer stem cells? Biochimica et Biophysica Acta 1795, 92–103.Google ScholarPubMed
Vicogne, J., Cailliau, K., Tulasne, D., Browaeys, E., Yan, Y. T., Fafeur, V., Vilain, J. P., Legrand, D., Trolet, J. and Dissous, C. (2004). Conservation of epidermal growth factor receptor function in the human parasitic helminth Schistosoma mansoni. Journal of Biological Chemistry 279, 37407–37414.CrossRefGoogle ScholarPubMed
Villegas, J., Araya, P., Bustos-Obregon, E. and Burzio, L. (2002). Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells. Molecular Human Reproduction 8, 977–983.Google Scholar
Vogel, H. (1977). Über den Echinococcus multilocularis Süddeutschlands. II. Entwicklung der Larvenstadien und histopathologische Reaktionen in der Feldmaus, Microtus arvalis. Tropenmedizin und Parasitologie 28, 409–427.Google ScholarPubMed
Wellinghausen, N., Gebert, P. and Kern, P. (1999). Interleukin (IL)−4, IL-10 and IL-12 profile in serum of patients with alveolar echinococcosis. Acta Tropica 73, 165–174.CrossRefGoogle ScholarPubMed
Wippersteg, V., Kapp, K., Kunz, W., Jackstadt, W. P., Zahner, H. and Grevelding, C. G. (2002). HSP70-controlled GFP expression in transiently transformed schistosomes. Molecular and Biochemical Parasitology 120, 141–150.Google Scholar
Xu, C. P., Ji, W. M., van den Brink, G. and Peppelenbosch, M. P. (2006). Bone morphogenetic protein-2 is a negative regulator of hepatocyte proliferation downregulated in the regenerating liver. World Journal of Gastroenterology 12, 7621–7625.CrossRefGoogle ScholarPubMed
Yang, X., Yang, C., Farberman, A., Rideout, T. C., de Lange, C. F., France, J. and Fan, M. Z. (2008). The mammalian target of rapamycin-signaling pathway in regulating metabolism and growth. Journal of Animal Science 86, E36–E50.CrossRefGoogle ScholarPubMed
Yokota, S. (2008). Historical survey on chromatoid body research. Acta Histochemica et Cytochemica 41, 65–82.CrossRefGoogle ScholarPubMed
Yoshida-Kashikawa, M., Shibata, N., Takechi, K. and Agata, K. (2007) DjCBC-1, a conserved DEAD box RNA helicase of the RCK/p54/Me31B family, is a component of RNA-protein complexes in planarian stem cells and neurons. Developmental Dynamics 236, 3436–3450.CrossRefGoogle ScholarPubMed
Zavala-Gongora, R., Kroner, A., Wittek, B., Knaus, P. and Brehm, K. (2003). Identification and characterization of two distinct Smad proteins from the fox-tapeworm Echinococcus multilocularis. International Journal for Parasitology 33, 1665–1677.Google Scholar
Zavala-Gongora, R., Derrer, B., Gelmedin, V., Knaus, P. and Brehm, K. (2008). Molecular characterization of a second structurally unusual AR-Smad without an MH1 domain and a Smad4 orthologue from Echinococcus multilocularis. International Journal for Parasitology 38, 161–176.CrossRefGoogle Scholar
Zavala-Gongora, R., Kroner, A., Bernthaler, P., Knaus, P. and Brehm, K. (2006). A member of the transforming growth factor-β receptor family from Echinococcus multilocularis is activated by human bone morphogenetic protein 2. Molecular and Biochemical Parasitology 146, 265–271.CrossRefGoogle ScholarPubMed
Zayas, R. M., Bold, T. D. and Newmark, P. A. (2005). Spliced-leader trans-splicing in freshwater planarians. Molecular Biology and Evolution 22, 2048–2054.CrossRefGoogle ScholarPubMed