Recent advances in the in vitro cultivation and genetic manipulation of Echinococcus multilocularis metacestodes and germinal cells

Experimental Parasitology

Volumn 119, Issue 4, 2008, Pages 506-515

  Brehm, Klaus ^a   Spiliotis, Markus ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cestode; Echinococcus; Germinal cells; Hymenolepis; In vitro cultivation; Mesocestoides; Neoblasts; Regeneration; Taenia; Transfection

Indexed keywords

CELL AGGREGATION; CELL DIFFERENTIATION; CELL PROLIFERATION; ECHINOCOCCUS GRANULOSUS; ECHINOCOCCUS MULTILOCULARIS; GENETIC MANIPULATION; GENETIC TRAIT; GERM CELL; IN VITRO STUDY; MEMBRANE VESICLE; METACESTODE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPECIES CULTIVATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CULTURE TECHNIQUES; ECHINOCOCCOSIS, HEPATIC; ECHINOCOCCUS MULTILOCULARIS; HUMANS; LARVA;

CESTODA; ECHINOCOCCUS; ECHINOCOCCUS MULTILOCULARIS; HYMENOLEPIS (CESTODA); MAMMALIA; MESOCESTOIDES; RODENTIA; TAENIA; VERMES;

EID: 46749097155     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2008.03.007     Document Type: Review

References (83)

1. Aguilar-Diaz H., Bobes R.J., Carrero J.C., Camacho-Carranza R., Cervantes C., Cevallos M.A., Davila G., Rodriguez-Dorantes M., Escobedo G., Fernandez J.L., Fragoso G., Gaytan P., Carciarubio A., Gonzalez V.M., Gonzalez L., Jose M.V., Jimenez L., Laclette J.P., Landa A., Larralde C., Morales-Montor J., Morett E., Ostoa-Saloma P., Sciutto E., Santamaria R.I., Soberon X., de la Torre P., Valdes V., and Yanez J. The genome project of Taenia solium. Parasitology International 55 (2006) S127-S130
2. Aldridge J.R., Jennette M.A., and Kuhn R.E. Uptake and secretion of host proteins by Taenia crassiceps metacestodes. Journal of Parasitology 92 (2006) 1101-1102
3. Ali-Khan Z., Siboo R., Gomersall M., and Faucher M. Cystolytic events and the possible role of germinal cells in metastasis in chronic alveolar hydatidosis. Annals of Tropical Medicine and Parasitology 77 (1983) 497-512
4. Ambrosio J., Landa A., Merchant M.T., and Laclette J.P. Protein uptake by cysticerci of Taenia crassiceps. Archives of Medical Research 25 (1994) 325-330
5. Bender R.C., Bixler L.M., Lerner J.P., and Bayne C.J. Schistosoma mansoni sporocysts in culture: host plasma hemoglobin contributes to in vitro oxidative stress. Journal of Parasitology 88 (2002) 14-18
6. Berezikov E., Bargmann C.I., and Plasterk R.H.A. Homologous gene targeting in Caenorhabditis elegans by biolistic transformation. Nucleic Acids Research 32 (2004) e40
7. 2 environments. Journal of Parasitology 87 (2001) 1167-1168
8. Brehm K., Jensen K., Frosch P., and Frosch M. Characterization of the genomic locus expressing the ERM-like protein of Echinococcus multilocularis. Molecular and Biochemical Parasitology 100 (1999) 147-152
9. Brehm K., Jensen K., and Frosch M. mRNA trans-splicing in the human parasitic cestode Echinococcus multilocularis. The Journal of Biological Chemistry 275 (2000) 38311-38318
10. Brehm K., Wolf M., Beland H., Kroner A., and Frosch M. Analysis of differential gene expression in Echinococcus multilocularis larval stages by means of spliced leader differential display. International Journal for Parasitology 33 (2003) 1145-1159
11. Brehm K., Spiliotis M., Zavala-Gongora R., Konrad C., and Frosch M. The molecular mechanisms of larval cestode development: first steps into an unknown world. Parasitology International 55 (2006) S15-S21
12. 2. Parasitology International 54 (2005) 185-193
13. Deplazes P., and Gottstein B. A monocylonal antibody against Echinococcus multilocularis Em2 antigen. Parasitology 103 (1991) 41-49
14. Dieckmann A., and Frank W. Isolation of viable germinal cells from Echinococcus multilocularis. Parasitology Research 74 (1988) 297-298
15. Dietrich G., Bubert A., Gentschev I., Sokolovic Z., Simm A., Catic A., Kaufmann S.H.E., Hess J., Szalay A.A., and Goebel W. Delivery of antigen-encoding plasmid DNA into the cytosol of macrophages by attenuated suicide Listeria monoytogenes. Nature Biotechnology 16 (1998) 181-185
16. Eckert J., Thompson R.C.A., and Mehlhorn H. Proliferation and metastases formation of larval Echinococcus multilocularis I. Animal model, macroscopical and hisatological findings. Zentralblatt für Parasitenkunde 69 (1983) 749-763
17. Fiori P.L., Monaco G., Scappaticci S., Pugliese A., Canu N., and Cappuccinelli P. Establishment of cell cultures from hydatid cysts of Echinococcus granulosus. International Journal for Parasitology 18 (1988) 297-305
18. Freeman R.S. Ontogeny of cestodes and its bearing on their phylogeny and systematics. Advances in Parasitology 11 (1973) 481-557
19. Freire T., Fernandez C., Chalar C., Maizels R.M., Alzari P., Osinaga E., and Robello C. Characterization of a UDP-N-acetyl-d-galactosmine:polypeptide N-acetylgalactosaminyltransferase with a unusual lectin domain from the platyhelminth parasite Echinococcus granulosus. Biochemical Journal 382 (2004) 501-510
20. Furuya K. An established cell line of larval Echinococcus multilocularis. International Journal for Parasitology 21 (1991) 233-240
21. Geldhof P., Visser A., Clark D., Saunders G., Britton C., Gilleard J., Berriman M., and Knox D. RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134 (2007) 609-619
22. Gelmedin V., Zavala-Gongora R., Fernandez C., and Brehm K. Echinococcus multilocularis: cloning and characterization of a member of the SNW/SKIP family of transcriptional coregulators. Experimental Parasitology 111 (2005) 115-120
23. Gimba E.R., Chemale G., Farias S.S., and Zaha A. Cloning and characterization of Echinococcus granulosus (Cestode) EgactI and EgactII actin gene promoters and their functional analysis in the NIH3T3 mouse cell line. Brazilian Journal of Medical and Biological Research 33 (2000) 1283-1292
24. Gonzalez-Estevez C., Momose T., Gehring W.J., and Salo E. Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proceedings of the National Academy of Sciences USA 100 (2003) 14046-14051
25. Gottstein B., Deplazes P., and Aubert M. Echinococcus multilocularis: immunological study on the "Em2-positive" laminated layer during in vitro and in vivo post-oncospheral and larval development. Parasitology Research 78 (1992) 291-297
26. Gregory T.R., Nicol J.A., Tamm H., Kullman B., Kullman K., Leitch I.J., Murray B.G., Kapraun D.F., Greilhuber J., and Bennett M.D. Eukaryotic genome size databases. Nucleic Acids Research 35 (2007) D332-D338
27. Grevelding C.G. Transgenic flatworms. In: Maule A.G., and Marks N.J. (Eds). Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (2006), CAB International 149-173
28. Heath D.D. An improved technique for the in vitro culture of taeniid larvae. International Journal for Parasitology 3 (1973) 481-484
29. Heath D.D., and Osborn P.J. Formation of Echinococcus granulosus laminated membrane in a defined medium. International Journal for Parasitology 6 (1976) 467-471
30. Hemphill A., and Gottstein B. Immunology and morphology studies on the proliferation of in vitro cultivated Echinococcus multilocularis metacestodes. Parasitology Research 81 (1995) 605-614
31. Hemphill A., Stettler M., Walker M., Siles-Lucas M., Fink R., and Gottstein B. Culture of Echinococcus multilocularis: an alternative to animal use. Trends in Parasitology 18 (2002) 445-451
32. Hemphill A., Stettler M., Walker M., Siles-Lucas M., Fink R., and Gottstein B. In vitro culture of Echinococcus multilocularis and Echinococcus vogeli metacestodes: studies on the host-parasite interface. Acta Tropica 85 (2003) 145-155
33. Hemphill A., Spicher M., Stadelmann B., Mueller J., Naguleswaran A., Gottstein B., and Walker M. Innovative chemotherapeutical treatment options for alveolar and cystic echinococcosis. Parasitology 134 (2007) 1657-1670
34. Holcman B., Heath D.D., and Shaw R.J. Ultrastructure of oncosphere and early stages of metacestode development of Echinococcus granulosus. International Journal for Parasitology 24 (1994) 623-635
35. Howell M.J., and Matthaei K. Points in question: In vitro culture of host or parasite cells. International Journal for Parasitology 18 (1988) 883-884
36. Howell M.J., and Smyth J.D. Maintenance and cultivation of Echinococcus species in vivo and in vitro. In: Thompson R.C.A., and Lymbery A.J. (Eds). Echinococcus and Hydatid Disease (1995), CAB International, Wallingford, Oxon, UK 201-232
37. Ivanchenko M.G., Lerner J.P., McCormick R.S., Toumadje A., Allen B., Fischer K., Hedstrom O., Helmrich A., Barnes D.W., and Bayne C.J. Continuous in vitro propagation and differentiation of cultures of the intramolluscan stages of the human parasite Schistosoma mansoni. Proceedings of the National Academy of Sciences USA 96 (1999) 4965-4970
38. Jimenez P., Valdez R.A., and Romano M.C. Metabolism of steroid hormones by Taenia solium and Taenia crassiceps cysticerci. Journal of Steroid Biochemistry and Molecular Biology 99 (2006) 203-208
39. Jura H., Bader A., Hartmann M., Maschek H., and Frosch M. Hepatic tissue culture model for study of host-parasite interactions in alveolar echinococcosis. Infection and Immunity 64 (1996) 3484-3490
40. Kamiya M., and Sato H. Complete life cycle of the canid tapeworm, Echinococcus multilocularis, in laboratory rodents. The FASEB Journal 4 (1990) 3334-3339
41. Kapel C.M.O., Torgerson P.R., Thompson R.C.A., and Deplazes P. Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats. International Journal for Parasitology 36 (2006) 79-86
42. Konrad C., Kroner A., Spiliotis M., Zavala-Gongora R., and Brehm K. Identification and molecular characterisation of a gene encoding a member of the insulin receptor family in Echinococcus multilocularis. International Journal for Parasitology 33 (2003) 301-312
43. Li C.X., Parker A., Menocal E., Xiang S., Borodyansky L., and Fruehauf J.H. Delivery of RNA interference. Cell Cycle 5 (2006) 2103-2109
44. Markoski M.M., Bizarro C.V., Farias S., Espinoza I., Galanti N., Zaha A., and Ferreira H.B. In vitro segmentation induction of Mesocestoides corti (Cestoda) tetrahyridia. Journal of Parasitology 89 (2003) 27-34
45. Martinez C., Paredes R., Stock R.P., Saralegui A., Andreu M., Cabezon C., Ehrlich R., and Galanti N. Cellular organization and appearance of differentiated structures in developing stages of the parasitic platyhelminth Echinococcus granulosus. Journal of Cellular Biochemistry 94 (2005) 327-335
46. Matsumoto J., Sakamoto K., Shinjyo N., Kido Y., Yamamoto N., Yagi K., Miyoshi H., Nonaka N., Katakura K., Kita K., and Oku Y. Anaerobic NADH-fumarate reductase system is predominant in the respiratory chain of Echinococcus multilocularis, providing a novel target for the chemotherapy of alveolar echinococcosis. Antimicrobial Agents and Chemotherapy 52 (2008) 164-170
47. Mehlhorn H., Eckert J., and Thompson R.C.A. Proliferation and metastases formation of larval Echinococcus multilocularis II. Ultrastructural investigations. Zentralblatt für Parasitenkunde 69 (1983) 749-763
48. Molina-Lopez J., Jimenez L., Ochoa-Sanchez A., and landa A. Molecular cloning and characterization of a 2-Cys peroxiredoxin from Taenia solium. Journal of Parasitology 92 (2006) 796-802
49. Morales M.E., Mann V.H., Kines K.J., Gobert G.N., Fraser M.J., Kalinna B.H., Correnti J.M., Pearce E.J., and Brindley P.J. piggyBac transposon mediated transgenesis of the human blood fluke Schistosoma mansoni. FASEB Journal 21 (2007) 3479-3489
50. Ndegewa D., Krautz-Peterson G., and Skelly P.J. Protocols for gene silencing in schistosomes. Experimental Parasitology 117 (2007) 284-291
51. Olson P.D. Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitology International 57 (2008) 8-17
52. Rausch R. Studies on the helminth fauna of Alaska. XX. The histogenesis of the alveolar larva of Echinococcus species. Journal of Infectious Disease 94 (1954) 178-186
53. Reuter M., and Kreshchenko N. Flatworm asexual multiplication implicates stem cells and regeneration. Canadian Journal of Zoology 82 (2004) 334-356
54. Rodriguez-Caabeiro F., and Casado N. Evidence of in vitro germinal layer development in Echinococcus granulosus cysts. Parasitology Research 74 (1988) 558-562
55. Rossi L., Salvetti A., Batistoni R., Deri P., and Gremigni V. Planarians, a tale of stem cells. Cellular and Molecular Life Sciences 65 (2008) 16-23
56. Sakamoto T., and Sugimura M. Studies on Echinococcus XXII: Electron microscopical observations on histogenesis of larval Echinococcus multilocularis. Japanese Journal of Veterinary Research 18 (1970) 131-144
57. Salinas G., Fernandez V., Fernandez C., and Selkirk M.E. Echinococcus granulosus: cloning of a thioredoxin peroxidase. Experimental Parasitology 90 (1998) 298-301
58. Sanchez-Alvarado A., and Kang H. Multicellularity, stem cells, and the neoblasts of the planarian Schmidtea mediterranea. Experimental Cell Research 306 (2005) 299-308
59. Seidel J.S. The life cycle in vitro of Hymenolepis microstoma (Cestoda). Journal of Parasitology 61 (1975) 677-681
60. Seidel J.S., and Voge M. Axenic development of cysticercoids of Hymenolepis nana. Journal of Parasitology 61 (1975) 861-864
61. Schuster F.L., and Sullivan J.J. Cultivation of clinically significant hemoflagellates. Clinical Microbiology Reviews 15 (2002) 374-389
62. Siles-Lucas M., and Hemphill A. Cestode parasites: application of in vivo and in vitro models for studies on the host-parasite relationship. Advances in Parasitology 51 (2002) 133-230
63. Siles-Lucas M., and Gottstein B. The 14-3-3 protein: a key molecule in parasites as in other organisms. Trends in Parasitology 19 (2003) 575-581
64. Slais J. Functional morphology of cestode larvae. Advances in Parasitology 11 (1973) 395-480
65. Smyth J.D., Howkins A.B., and Barton M. Factors controlling the differentiation of the hydatid organism, Echinococcus granulosus, into cystic or strobilar stages. Nature 211 (1966) 1374-1377
66. Spiliotis M., Kroner A., and Brehm K. Identification, molecular characterization and expression of the gene encoding the epidermal growth factor receptor orthologue from the fox-tapeworm Echinococcus multilocularis. Gene 323 (2003) 57-65
67. Spiliotis M., and Brehm K. Echinococcus multilocularis: identification and molecular characterization of a Ral-like small GTP-binding protein. Experimental Parasitology 107 (2004) 163-172
68. Spiliotis M., Tappe D., Sesterhenn L., and Brehm K. Long-term in vitro cultivation of Echinococcus multilocularis metacestodes under axenic conditions. Parasitology Research 92 (2004) 430-432
69. Spiliotis M., Tappe D., Brückner S., Mösch H.U., and Brehm K. Molecular cloning and characterization of Ras- and Raf-homologues from the fox-tapeworm Echinococcus multilocularis. Molecular and Biochemical Parasitology 139 (2005) 225-237
70. Spiliotis M., Konrad C., Gelmedin V., Tappe D., Brückner S., Mösch H.U., and Brehm K. Characterisation 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 (2006) 1097-1112
71. Spiliotis, M., Brehm, K, 2008. Axenic in vitro cultivation of Echinococcus multilocularis metacestode vesicles and the generation of primary cell cultures. In: Rupp, Sohn, Hauser (Eds.). Methods in Molecular Biology; Host-Pathogen Interactions, vol. 470. Humana Press Inc.; in press.
72. Spiliotis, M., Lechner, S., Tappe, D., Scheller, C., Krohne, G., Brehm, K, 2008. Transient transfection of Echinococcus multilocularis primary cells and complete in vitro regeneration of metacestode vesicles. International Journal for Parasitology 38, in press.
73. Swiderski Z. Echinococcus granulosus: hook-muscle systems and cellular organisation of infective oncospheres. International Journal for Parasitology 13 (1983) 289-299
74. Thompson R.C.A. Biology and systematics of Echinococcus. In: Thompson R.C.A., and lymbery A.J. (Eds). Echinococcus and Hydatid Disease (1995), CAB International, Wallingford 1-50
75. Toledo A., Cruz C., Fragoso G., Laclette J.P., Merchant M.T., Hernandez M., and Sciutto E. In vitro culture of Taenia crassiceps larval cells and cyst regeneration after injection into mice. Journal of Parasitology 83 (1997) 189-193
76. Voge M., and Green J. Axenic growth of oncospheres of Hymenolepis citelli (Cestoda) to fully developed cysticercoids. Journal of Parasitology 61 (1975) 291-297
77. Voge M., Jaffe J., Bruckner D.A., and Meymarian E. Synergistic growth promoting action of l-cysteine and nitrogen upon Hymenolepis diminuta cysticercoids in vitro. Journal of Parasitology 62 (1976) 951-954
78. Vogel H. Über den Echinococcus multilocularis Süddeutschlands. II. Entwicklung der Larvenstadien und histopathologische Reaktionen in der Feldmaus Microtus arvalis. Tropenmedizin und Parasitologie 28 (1977) 409-560
79. Wilson J.F., Rausch R.L., and Wilson F.R. Alveolar hydatid disease: review of the surgical experience in 42 cases of active disease among Alaskan Eskimos. Annals of Surgery 221 (1995) 315-323
80. Yamashita K., Uchino J., Sato N., Furuya K., and Namieno T. Establishment of a primary culture of Echinococcus multilocularis cells. Journal of Gastroenterology 32 (1997) 344-350
81. Zavala-Gongora R., Kroner A., Wittek B., Knaus P., and Brehm K. Identification and characterisation of two distinct Smad proteins from the fox-tapeworm Echinococcus multilocularis. International Journal for Parasitology 33 (2003) 1665-1677
82. Zavala-Gongora R., Kroner A., Bernthaler P., Knaus P., and Brehm K. 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 (2006) 265-271
83. Zavala-Gongora R., Derrer B., Gelmedin V., Knaus P., and Brehm K. Molecular characterisation of a second structurally unusual AR-Smad without an MH1 domain and a Smad4 orthologue from Echinococcus multilocularis. International Journal for Parasitology 38 (2008) 161-176