Skip to main content Accessibility help

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

  • K. BREHM (a1)


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.


Corresponding author

*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:


Hide All
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, 497512.
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.
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, 91339138.
Amikura, R., Sato, K. and Kobayashi, S. (2005). Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mechanisms of Development 122, 10871093.
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, 7680.
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, 19331939.
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, 3161331619.
Botero, D. (1970). Paromomycin as effective treatment of Taenia infections. American Journal of Tropical Medicine and Hygiene 19, 234237.
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, 105110.
Brehm, K., Jensen, K. and Frosch, M. (2000 a). mRNA trans-splicing in the human parasitic cestode Echinococcus multilocularis. Journal of Biological Chemistry 275, 3831138318.
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, 297302.
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, 506515.
Brehm, K. and Spiliotis, M. (2008 b). The influence of host hormones and cytokines on Echinococcus multilocularis signalling and development. Parasite 15, 286290.
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, S15S21.
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, 11451159.
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, 399408.
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.
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, 733743.
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, 8388.
Coustau, C. and Yoshino, T. P. (2000) Flukes without snails: advances in the in vitro cultivation of intramolluscan stages of trematodes. Experimental Parasitology 94, 6266.
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, 2181321819.
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, 2002620030.
Delcuve, G. P., Rastegar, M. and Davie, J. R. (2009). Epigenetic control. Journal of Cellular Physiology 219, 243250.
Dowling, R. J., Pollak, M. and Sonenberg, N. (2009). Current status and challenges associated with targeting mTOR for cancer therapy. BioDrugs 23, 7791.
Drummond-Barbosa, D. (2008). Stem cells, their niches and the systemic environment: an aging network. Genetics 180, 17871797.
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, 327339.
Fausto, N. (2000). Liver regeneration. Journal of Hepatology 32, 1931.
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, 171180.
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, 294303.
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, 29.
Gangaraju, V. K. and Lin, H. (2009). MicroRNAs: key regulators of stem cells. Nature Reviews Molecular Cell Biology 10, 116125.
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, 10681081.
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.2009.10.009
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, 115120.
Gilleard, J. S. (2004). The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 128, S49S70.
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, 64026410.
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, 159169.
Guo, X. and Wang, X. F. (2009). Signaling cross-talk between TGF-β/BMP and other pathways. Cell Research 19, 7188.
Gur, Y. and Breitbart, H. (2008). Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Molecular and Cellular Endocrinology 282, 4555.
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, 157167.
Hamilton, T. L., Stoneley, M., Spriggs, K. A. and Bushell, M. (2006). TOPs and their regulation. Biochemical Society Transactions 34, 1216.
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, 231236.
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, 621629.
Heath, D. D. and Lawrence, S. B. (1976). Echinococcus granulosus: development in vitro from oncosphere to immature hydatid cyst. Parasitology 73, 417423.
Hemphill, A. and Gottstein, B. (1995). Immunology and morphology studies on the proliferation of in vitro cultivated Echinococcus multilcoularis metacestodes. Parasitology Research 81, 605614.
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, 571581.
Hori, I. (1982). An ultrastructural study of the chromatoid body in planarian regenerative cells. Journal of Electron Microscopy 31, 6372.
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, 29.
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, 209226.
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, 34843490.
Kaiser, P., Rothwell, L., Avery, S. and Balu, S. (2004). Evolution of the interleukins. Developmental and Comparative Immunology 28, 374394.
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, 7177.
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, 659676.
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, 29362948.
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, 706714.
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, 943954.
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, 301312.
Kotaja, N. and Sassone-Corsi, P. (2007). The chromatoid body: a germ-cell-specific RNA-processing centre. Nature Reviews Molecular Cell Biology 8, 8590.
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, 4557345585.
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, 475482.
Long, X., Müller, F. and Avruch, J. (2004). TOR action in mammalian cells and in Caenorhabditis elegans. Current Topics in Microbiology and Immunology 279, 115138.
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, 211216.
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.
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, 7582.
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.
Mehlhorn, H., Eckert, J. and Thompson, R. C. A. (1983). Proliferation and metastases formation of larval Echinococcus multilocularis. Zentralblatt für Parasitenkunde 69, 749763.
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, 953961.
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, 7994.
Morris, D. L. and Taylor, D. H. (1990). Echinococcus granulosus: development of resistance to albendazole in an animal model. Journal of Helminthology 64, 171174.
Morrison, S. J. and Spradling, A. C. (2008). Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132, 598611.
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, 9199.
Olson, P. D. (2008). Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitology International 57, 8–17.
Oviedo, N. J. and Beane, W. S. (2009). Regeneration: The origin of cancer as a possible cure? Seminars in Cell and Developmental Biology 20, 557564.
Oviedo, N. J. and Levin, M. (2007). smedinx-11 is a planarian stem cell gap junction gene required for regeneration and homeostasis. Development 134, 31213131.
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, 131143.
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, 11741186.
Pearce, E. J. and Freitas, T. C. (2008). Reverse genetics and the study of the immune response to schistosomes. Parasite Immunology 30, 215221.
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, 565572.
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, 178186.
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, 635649.
Reuter, M. and Kreshchenko, N. (2004). Flatworm asexual multiplication implicates stem cells and regeneration. Canadian Journal of Zoology 82, 334356.
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, 127140.
Rossi, L., Salvetti, A., Batistoni, R., Deri, P. and Gremigni, V. (2008). Planarians, a tale of stem cells. Cellular and Molecular Life Sciences 65, 1623.
Rybicka, K. (1966). Embryogenesis in cestodes. Advances in Parasitology 4, 107186.
Sakamoto, T. (1981). Electron microscopical observations on the egg of Echinococcus multilocularis. Memoirs of the Faculty of Agriculture, Kagoshima University 17, 165174.
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, 127139.
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, 131144.
Saló, E. (2006). The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). BioEssays 28, 546559.
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, 13171327.
Saló, E. and Baguna, J. (2002). Regeneration in planarians and other worms: new findings, new tools, and new perspectives. Journal of Experimental Zoology 292, 528539.
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, 603614.
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, 18631874.
Sanchez-Alvarado, A. (2006). Planarian regeneration: its end and its beginning. Cell 124, 241245.
Sanchez-Alvarado, A. and Kang, H. (2005). Multicellularity, stem cells, and the neoblast of the planarian Schmidtea mediterranea. Experimental Cell Research 306, 299308.
Sánchez-Alvarado, A. and Tsonis, P. A. (2006). Bridging the regeneration gap: genetic insights from diverse animal models. Nature Reviews Genetics 7, 873884.
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, 615628.
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, 107114.
Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature 441, 10751079.
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, 123130.
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, 7387.
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, 11241129.
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, 133230.
Slais, J. (1973) Functional morphology of cestode larvae. Advances in Parasitology 11, 395480.
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, 410421.
Spiliotis, M. and Brehm, K. (2004). Echinococcus multilocularis: identification and molecular characterization of a Ral-like small GTP-binding protein. Experimental Parasitology 107, 163172.
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, 245262.
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, 10971112.
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, 5765.
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, 10251039.
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, 225237.
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, 430432.
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.
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, 256264.
Swiderski, Z. (1983) Echinococcus granulosus: hook-muscle systems and cellular organisation of infective oncospheres. International Journal for Parasitology 13, 289299.
Tanaka, E. M. and Weidinger, G. (2008). Heads or tails: can Wnt tell which one is up? Nature Cell Biology 10, 122124.
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, 504506.
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, 138147.
Tysnes, B. B. and Bjerkvig, R. (2007). Cancer initiation and progression: involvement of stem cells and the microenvironment. Biochimica et Biophysica Acta 1775, 283297.
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.
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, 3740737414.
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, 977983.
Vogel, H. (1977). Über den Echinococcus multilocularis Süddeutschlands. II. Entwicklung der Larvenstadien und histopathologische Reaktionen in der Feldmaus, Microtus arvalis. Tropenmedizin und Parasitologie 28, 409427.
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, 165174.
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, 141150.
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, 76217625.
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, E36E50.
Yokota, S. (2008). Historical survey on chromatoid body research. Acta Histochemica et Cytochemica 41, 6582.
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, 34363450.
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, 16651677.
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, 161176.
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, 265271.
Zayas, R. M., Bold, T. D. and Newmark, P. A. (2005). Spliced-leader trans-splicing in freshwater planarians. Molecular Biology and Evolution 22, 20482054.


Related content

Powered by UNSILO

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

  • K. BREHM (a1)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.