Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-31T06:41:22.016Z Has data issue: false hasContentIssue false
  • English
  • Français

Cell repertoire and proliferation of germinative cells of the model cestode Mesocestoides corti

Published online by Cambridge University Press:  05 July 2022

María Fernanda Domínguez ,
Alicia Costábile ,
Uriel Koziol ,
Matías Preza ,
Klaus Brehm ,
José F. Tort  and
Estela Castillo Open the ORCID record for Estela Castillo [Opens in a new window]
María Fernanda Domínguez
Affiliation:
Departamento de Genética, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay
Alicia Costábile
Affiliation:
Sección Bioquímica, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay
Uriel Koziol
Affiliation:
Sección Biología Celular, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay
Matías Preza
Affiliation:
Sección Biología Celular, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay
Klaus Brehm
Affiliation:
University of Würzburg, Institute of Hygiene and Microbiology, Würzburg, Germany
José F. Tort
Affiliation:
Departamento de Genética, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay
Estela Castillo*
Affiliation:
Sección Bioquímica, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay
*
Author for correspondence: Estela Castillo, E-mail: castillo@fcien.edu.uy
Get access Rights & Permissions [Opens in a new window]

Abstract

The phylum Platyhelminthes shares a unique population of undifferentiated cells responsible for the proliferation capacity needed for cell renewal, growth, tissue repair and regeneration. These cells have been extensively studied in free-living flatworms, whereas in cestodes the presence of a set of undifferentiated cells, known as germinative cells, has been demonstrated in classical morphology studies, but poorly characterized with molecular biology approaches. Furthermore, several genes have been identified as neoblast markers in free-living flatworms that deserve study in cestode models. Here, different cell types of the model cestode Mesocestoides corti were characterized, identifying differentiated and germinative cells. Muscle cells, tegumental cells, calcareous corpuscle precursor cells and excretory system cells were identified, all of which are non-proliferative, differentiated cell types. Besides those, germinative cells were identified as a population of small cells with proliferative capacity in vivo. Primary cell culture experiments in Dulbecco's Modified Eagle Medium (DMEM), Echinococcus hydatid fluid and hepatocyte conditioned media in non-reductive or reductive conditions confirmed that the germinative cells were the only ones with proliferative capacity. Since several genes have been identified as markers of undifferentiated neoblast cells in free-living flatworms, the expression of pumilio and pL10 genes was analysed by qPCR and in situ hybridization, showing that the expression of these genes was stronger in germinative cells but not restricted to this cell type. This study provides the first tools to analyse and further characterise undifferentiated cells in a model cestode.

Keywords

Cell culturecell typescestodesgerminative cellsproliferation markers
Type
Research Article
Information
Parasitology , Volume 149 , Issue 11 , September 2022 , pp. 1505 - 1514
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aboobaker, AA (2011) Planarian stem cells: a simple paradigm for regeneration. Trends in Cell Biology 21, 304–311.CrossRefGoogle ScholarPubMed
Barrett, NJ, Smyth, JD and Ong, SJ (1982) Spontaneous sexual differentiation of Mesocestoides corti tetrathyridia in vitro. International Journal for Parasitology 12, 315–322.CrossRefGoogle ScholarPubMed
Bolla, RI and Roberts, LS (1971) Developmental physiology of cestodes. IX. Cytological characteristics of the germinative region of Hymenolepis diminuta. The Journal of Parasitology 57, 267–277.CrossRefGoogle ScholarPubMed
Brehm, K and Spiliotis, M (2008) Recent advances in the in vitro cultivation and genetic manipulation of Echinococcus multilocularis metacestodes and germinal cells. Experimental Parasitology 119, 506–515.CrossRefGoogle ScholarPubMed
Britos, L, Domínguez, L, Ehrlich, R and Marín, M (2000) Effect of praziquantel on the strobilar development of Mesocestoides corti in vitro. Journal of Helminthology 74, 295–299.CrossRefGoogle ScholarPubMed
Camargo de Lima, J, Monteiro, KM, Basika Cabrera, TN, Paludo, GP, Moura, H, Barr, JR, Zaha, A and Ferreira, HB (2018) Comparative proteomics of the larval and adult stages of the model cestode parasite Mesocestoides corti. Journal of Proteomics 175, 127–135.CrossRefGoogle ScholarPubMed
Cheng, Z, Liu, F, Dai, M, Wu, J, Li, X, Guo, X, Tian, H, Heng, Z, Lu, Y, Chai, X and Wang, Y (2017) Identification of EmSOX2, a member of the Sox family of transcription factors, as a potential regulator of Echinococcus multilocularis germinative cells. International Journal for Parasitology 47, 625–632.CrossRefGoogle ScholarPubMed
Coghlan, A, Tyagi, R, Cotton, JA, Holroyd, N, Rosa, BA, Tsai, IJ, Laetsch, DR, Beech, RN, Day, TA, Hallsworth-Pepin, K, Ke, H-M, Kuo, T-H, Lee, TJ, Martin, J, Maizels, RM, Mutowo, P, Ozersky, P, Parkinson, J, Reid, AJ, Rawlings, ND, Ribeiro, DM, Swapna, LS, Stanley, E, Taylor, DW, Wheeler, NJ, Zamanian, M, Zhang, X, Allan, F, Allen, JE, Asano, K, Babayan, SA, Bah, G, Beasley, H, Bennett, HM, Bisset, SA, Castillo, E, Cook, J, Cooper, PJ, Cruz-Bustos, T, Cuéllar, C, Devaney, E, Doyle, SR, Eberhard, ML, Emery, A, Eom, KS, Gilleard, JS, Gordon, D, Harcus, Y, Harsha, B, Hawdon, JM, Hill, DE, Hodgkinson, J, Horák, P, Howe, KL, Huckvale, T, Kalbe, M, Kaur, G, Kikuchi, T, Koutsovoulos, G, Kumar, S, Leach, AR, Lomax, J, Makepeace, B, Matthews, JB, Muro, A, O'Boyle, NM, Olson, PD, Osuna, A, Partono, F, Pfarr, K, Rinaldi, G, Foronda, P, Rollinson, D, Samblas, MG, Sato, H, Schnyder, M, Scholz, T, Shafie, M, Tanya, VN, Toledo, R, Tracey, A, Urban, JF, Wang, L-C, Zarlenga, D, Blaxter, ML, Mitreva, M, Berriman, M and International Helminth Genomes Consortium (2019) Comparative genomics of the major parasitic worms. Nature Genetics 51, 163–174.Google Scholar
Cordin, O, Banroques, J, Tanner, NK and Linder, P (2006) The DEAD-box protein family of RNA helicases. Gene 367, 17–37.CrossRefGoogle ScholarPubMed
Costábile, A, Marín, M and Castillo, E (2017) Spatio-temporal expression of Mesocestoides corti McVAL2 during strobilar development. Experimental Parasitology 181, 30–39.CrossRefGoogle ScholarPubMed
Costábile, A, Koziol, U, Tort, JF, Iriarte, A and Castillo, E (2018) Expansion of cap superfamily proteins in the genome of Mesocestoides corti: an extreme case of a general bilaterian trend. Gene Reports 11, 110–120.CrossRefGoogle Scholar
Curtis, D, Treiber, DK, Tao, F, Zamore, PD, Williamson, JR and Lehmann, R (1997) A CCHC metal-binding domain in Nanos is essential for translational regulation. The EMBO Journal 16, 834–843.CrossRefGoogle ScholarPubMed
David, CN (1973) A quantitative method for maceration of hydra tissue. Wilhelm Roux’ Archiv für Entwicklungsmechanik der Organismen 171, 259–268.CrossRefGoogle ScholarPubMed
Domínguez, MF, Koziol, U, Porro, V, Costábile, A, Estrade, S, Tort, J, Bollati-Fogolin, M and Castillo, E (2014) A new approach for the characterization of proliferative cells in cestodes. Experimental Parasitology 138, 25–29.CrossRefGoogle ScholarPubMed
Douglas, LT (1961) The development of organ systems in nematotaeniid cestodes. I. Early histogenesis and formation of reproductive structures in Baerietta diana (Helfer, 1948). The Journal of Parasitology 47, 669–680.CrossRefGoogle ScholarPubMed
Egger, B, Lapraz, F, Tomiczek, B, Müller, S, Dessimoz, C, Girstmair, J, Škunca, N, Rawlinson, KA, Cameron, CB, Beli, E, Todaro, MA, Gammoudi, M, Noreña, C and Telford, MJ (2015) A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Current Biology 25, 1347–1353.CrossRefGoogle ScholarPubMed
Etges, FJ (1991) The proliferative tetrathyridium of Mesocestoides vogae sp. N. (Cestoda). Journal of the Helminthological Society of Washington 58, 181–185.Google Scholar
Fincher, CT, Wurtzel, O, de Hoog, T, Kravarik, KM and Reddien, PW (2018) Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science 360, eaaq1736.CrossRefGoogle ScholarPubMed
Fontenla, S, Rinaldi, G, Smircich, P and Tort, JF (2017) Conservation and diversification of small RNA pathways within flatworms. BMC Evolutionary Biology 17, 215.CrossRefGoogle ScholarPubMed
Fontenla, S, Rinaldi, G and Tort, JF (2021) Lost and found: Piwi and Argonaute pathways in flatworms. Frontiers in Cellular and Infection Microbiology 11, 653695. doi: 10.3389/fcimb.2021.653695CrossRefGoogle ScholarPubMed
Förster, S, Koziol, U, Schäfer, T, Duvoisin, R, Cailliau, K, Vanderstraete, M, Dissous, C and Brehm, K (2019) The role of fibroblast growth factor signalling in Echinococcus multilocularis development and host-parasite interaction. PLoS Neglected Tropical Diseases 13, e0006959.CrossRefGoogle ScholarPubMed
Garcia, HH, Moro, PL and Schantz, PM (2007) Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Current Opinion in Infectious Diseases 20, 489–494.CrossRefGoogle ScholarPubMed
Gee, SL and Conboy, JG (1994) Mouse erythroid cells express multiple putative RNA helicase genes exhibiting high sequence conservation from yeast to mammals. Gene 140, 171–177.CrossRefGoogle ScholarPubMed
Gorbalenya, AE and Koonin, EV (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Current Opinion in Structural Biology 3, 419–429.CrossRefGoogle Scholar
Greenspan, P, Mayer, EP and Fowler, SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. Journal of Cell Biology 100, 965–973.CrossRefGoogle ScholarPubMed
Guo, T, Peters, AHFM and Newmark, PA (2006) A bruno-like gene is required for stem cell maintenance in planarians. Developmental Cell 11, 159–169.CrossRefGoogle ScholarPubMed
Gururajan, R, Perry-O'Keefet, H, Melton, DA and Weeks, DL (1991) The Xenopus localized messenger RNA An3 may encode an ATP-dependent RNA helicase. Nature 349, 717–719.CrossRefGoogle ScholarPubMed
Gustafsson, MKS (1976) Studies on cytodifferentiation in the neck region of Diphyllobothrium dendriticum Nitzsch, 1824 (Cestoda, Pseudophyllidea). Zeitschrift für Parasitenkunde 50, 323–329.CrossRefGoogle ScholarPubMed
Gustafsson, MK (1990) The cells of a cestode. Diphyllobothrium dendriticum as a model in cell biology. The early brain. Proceedings of a symposium on invertebrate neurobiology, MKS Gustafsson and M Reuter (eds). Acta AcademiaeAboensis 50, 13–44.Google Scholar
Hart, JL (1967) Studies on the nervous system of tetrathyridia (Cestoda: Mesocestoides). The Journal of Parasitology 53, 1032.CrossRefGoogle ScholarPubMed
Hay, ED and Coward, SJ (1975) Fine structure studies on the planarian, Dugesia: I. Nature of the ‘neoblast’ and other cell types in non injured worms. Journal of Ultrastructure Research 50, 1–21.CrossRefGoogle Scholar
Hemer, S, Konrad, C, Spiliotis, M, Koziol, U, Schaack, D, Förster, S, Gelmedin, V, Stadelmann, B, Dandekar, T, Hemphill, A and Brehm, K (2014) Host insulin stimulates Echinococcus multilocularis insulin signalling pathways and larval development. BMC Biology 12, 5.CrossRefGoogle ScholarPubMed
Hess, E (1980) Ultrastructural study of the tetrathyridium of Mesocestoides corti Hoeppli, 1925: tegument and parenchyma. Zeitschrift für Parasitenkunde Parasitology Research 61, 135–159.CrossRefGoogle ScholarPubMed
Hess, E (1981) Ultrastructural study of the tetrathyridium of Mesocestoides corti Hoeppli, 1925 (Cestoda): pool of germinative cells and suckers. Revue Suisse de Zoologie 88, 661–674.CrossRefGoogle Scholar
Hopman, AHN, Ramaekers, FCS and Speel, EJM (1998) Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for in situ hybridization using CARD amplification. Journal of Histochemistry & Cytochemistry 46, 771–777.CrossRefGoogle ScholarPubMed
Ikenishi, K and Tanaka, TS (1997) Involvement of the protein of Xenopus vasa homolog (Xenopus vasa-like gene 1, XVLG1) in the differentiation of primordial germ cells. Development, Growth & Differentiation 39, 625–633.CrossRefGoogle ScholarPubMed
Johnstone, O, Deuring, R, Bock, R, Linder, P, Fuller, MT and Lasko, P (2005) Belle is a Drosophila DEAD-box protein required for viability and in the germ line. Developmental Biology 277, 92–101.CrossRefGoogle Scholar
Juliano, CE, Swartz, SZ and Wessel, GM (2010) A conserved germline multipotency program. Development 137, 4113–4126.CrossRefGoogle ScholarPubMed
Koziol, U and Castillo, E (2011) Cell proliferation and differentiation in cestodes. In Esteves, A (ed.), Research in Helminths. Kerala, India: Transworld Research Network, pp. 121–138.Google Scholar
Koziol, U, Marín, M and Castillo, E (2008) Pumilio genes from the Platyhelminthes. Development Genes and Evolution 218, 47–53.CrossRefGoogle ScholarPubMed
Koziol, U, Domínguez, MF, Marín, M, Kun, A and Castillo, E (2010) Stem cell proliferation during in vitro development of the model cestode Mesocestoides corti from larva to adult worm. Frontiers in Zoology 7, 22.CrossRefGoogle ScholarPubMed
Koziol, U, Krohne, G and Brehm, K (2013) Anatomy and development of the larval nervous system in Echinococcus multilocularis. Frontiers in Zoology 10, 24.CrossRefGoogle ScholarPubMed
Koziol, U, Rauschendorfer, T, Rodríguez, LZ, Krohne, G and Brehm, K (2014) The unique stem cell system of the immortal larva of the human parasite Echinococcus multilocularis. EvoDevo 5, 10.CrossRefGoogle ScholarPubMed
Koziol, U, Radio, S, Smircich, P, Zarowiecki, M, Fernández, C and Brehm, K (2015) A novel terminal-repeat retrotransposon in miniature (TRIM) is massively expressed in Echinococcus multilocularis stem cells. Genome Biology and Evolution 7, 2136–2153.CrossRefGoogle Scholar
Kurisaki, I, Iwai, T, Yamashita, M, Kobayashi, M, Ito, E and Matsuoka, I (2007) Identification and expression analysis of rainbow trout pumilio-1 and pumilio-2. Cell and Tissue Research 327, 33–42.CrossRefGoogle ScholarPubMed
Kuznicki, KA, Smith, PA, Leung-Chiu, WM, Estevez, AO, Scott, HC and Bennett, KL (2000) Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 127, 2907–2916.CrossRefGoogle ScholarPubMed
Lascano, EF, Coltorti, EA and Varela-Díaz, VM (1975) Fine structure of the germinal membrane of Echinococcus granulosus cysts. The Journal of Parasitology 61, 853–860.CrossRefGoogle ScholarPubMed
Lasko, PF and Ashburner, M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611–617.CrossRefGoogle ScholarPubMed
Linder, P (2010) Chapter 2: the dynamic life with DEAD-box RNA helicases. In Jankowsky, E (ed.), RNA Helicases. Cambridge: RSC Biomolecular Sciences, pp. 32–60.CrossRefGoogle Scholar
Linder, P and Jankowsky, E (2011) From unwinding to clamping – the DEAD box RNA helicase family. Nature Reviews Molecular Cell Biology 12, 505–516.CrossRefGoogle ScholarPubMed
Loehr, KA and Mead, RW (1979) A maceration technique for the study of cytological development in Hymenolepis citelli. The Journal of Parasitology 65, 886–889.CrossRefGoogle Scholar
Moore, FL, Jaruzelska, J, Fox, MS, Urano, J, Firpo, MT, Turek, PJ, Dorfman, DM and Pera, RAR (2003) Human pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proceedings of the National Academy of Sciences 100, 538–543.CrossRefGoogle ScholarPubMed
Morita, M, Best, JB and Noel, J (1969) Electron microscopic studies of planarian regeneration. I. Fine structure of neoblasts in Dugesia dorotocephala. Journal of Ultrastructure Research 27, 7–23.CrossRefGoogle ScholarPubMed
Ogawa, K, Kobayashi, C, Hayashi, T, Orii, H, Watanabe, K and Agata, K (2002) Planarian fibroblast growth factor receptor homologs expressed in stem cells and cephalic ganglions. Development, Growth and Differentiation 44, 191–204.CrossRefGoogle ScholarPubMed
Ohashi, H, Umeda, N, Hirazawa, N, Ozaki, Y, Miura, C and Miura, T (2007) Expression of vasa (vas)-related genes in germ cells and specific interference with gene functions by double-stranded RNA in the monogenean, Neobenedenia girellae. International Journal for Parasitology 37, 515–523.CrossRefGoogle ScholarPubMed
Olsen, LC, Aasland, R and Fjose, A (1997) A vasa-like gene in zebrafish identifies putative primordial germ cells. Mechanisms of Development 66, 95–105.CrossRefGoogle ScholarPubMed
Önal, P, Grün, D, Adamidi, C, Rybak, A, Solana, J, Mastrobuoni, G, Wang, Y, Rahn, H-P, Chen, W, Kempa, S, Ziebold, U and Rajewsky, N (2012) Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells: conserved determinants of planarian pluripotency. The EMBO Journal 31, 2755–2769.CrossRefGoogle ScholarPubMed
Ong, SJ and Smyth, JD (1986) Effects of some culture factors on sexual differentiation of Mesocestoides corti grown from tetrathyridia in vitro. International Journal for Parasitology 16, 361–368.CrossRefGoogle ScholarPubMed
Peter, R, Gschwentner, R, Schürmann, W, Rieger, RM and Ladurner, P (2004) The significance of stem cells in free-living flatworms: one common source for all cells in the adult. Journal of Applied Biomedicine 2, 21–35.CrossRefGoogle Scholar
Plass, M, Solana, J, Wolf, FA, Ayoub, S, Misios, A, Glažar, P, Obermayer, B, Theis, FJ, Kocks, C and Rajewsky, N (2018) Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. Science 360, eaaq1723.CrossRefGoogle ScholarPubMed
Reddien, PW (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310, 1327–1330.CrossRefGoogle ScholarPubMed
Reuter, M and Kreshchenko, N (2004) Flatworm asexual multiplication implicates stem cells and regeneration. Canadian Journal of Zoology 82, 334–356.CrossRefGoogle Scholar
Rink, JC (2013) Stem cell systems and regeneration in planaria. Development Genes and Evolution 223, 67–84.CrossRefGoogle ScholarPubMed
Rossi, L, Salvetti, A, Batistoni, R, Deri, P and Gremigni, V (2008) Molecular and cellular basis of regeneration and tissue repair: planarians, a tale of stem cells. Cellular and Molecular Life Sciences 65, 16–23.CrossRefGoogle Scholar
Rouhana, L, Shibata, N, Nishimura, O and Agata, K (2010) Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance. Developmental Biology 341, 429–443.CrossRefGoogle ScholarPubMed
Rozario, T, Quinn, EB, Wang, J, Davis, RE and Newmark, PA (2019) Region-specific regulation of stem cell-driven regeneration in tapeworms. eLife 8, e48958.CrossRefGoogle ScholarPubMed
Sakamoto, T and Sugimura, M (1970) [Studies on echinococcosis. XXIII. Electron microscopical observations on histogenesis of larval Echinococcus multilocularis]. Japanese Journal of Veterinary Research 18, 31–44.Google Scholar
Salvetti, A, Rossi, L, Lena, A, Batistoni, R, Deri, P, Rainaldi, G, Locci, M, 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
Shibata, N, Umesono, 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
Skinner, DE, Rinaldi, G, Suttiprapa, S, Mann, VH, Smircich, P, Cogswell, AA, Williams, DL and Brindley, PJ (2012) Vasa-like DEAD-Box RNA helicases of Schistosoma mansoni. PLoS Neglected Tropical Diseases 6, e1686.CrossRefGoogle ScholarPubMed
Skinner, DE, Rinaldi, G, Koziol, U, Brehm, K and Brindley, PJ (2014) How might flukes and tapeworms maintain genome integrity without a canonical piRNA pathway? Trends in Parasitology 30, 123–129.CrossRefGoogle ScholarPubMed
Specht, D and Voge, M (1965) Asexual multiplication of Mesocestoides tetrathyridia in laboratory animals. The Journal of Parasitology 51, 268.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
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
Sulgostowska, T (1972) The development of organ systems in cestodes I: a study of histology of Hymenolepis diminuta (Rudolphi, 1819). Acta Parasitologica Polonica 20, 449–642.Google Scholar
Swapna, LS, Molinaro, AM, Lindsay-Mosher, N, Pearson, BJ and Parkinson, J (2018) Comparative transcriptomic analyses and single-cell RNA sequencing of the freshwater planarian Schmidtea mediterranea identify major cell types and pathway conservation. Genome Biology 19, 124.CrossRefGoogle ScholarPubMed
Thompson, RCA, Jue Sue, LP and Buckley, SJ (1982) In vitro development of the strobilar stage of Mesocestoides corti. International Journal for Parasitology 12, 303–314.CrossRefGoogle ScholarPubMed
Tsai, IJ, Zarowiecki, M, Holroyd, N, Garciarrubio, A, Sanchez-Flores, A, Brooks, KL, Tracey, A, Bobes, RJ, Fragoso, G, Sciutto, E, Aslett, M, Beasley, H, Bennett, HM, Cai, J, Camicia, F, Clark, R, Cucher, M, De Silva, N, Day, TA, Deplazes, P, Estrada, K, Fernández, C, Holland, PWH, Hou, J, Hu, S, Huckvale, T, Hung, SS, Kamenetzky, L, Keane, JA, Kiss, F, Koziol, U, Lambert, O, Liu, K, Luo, X, Luo, Y, Macchiaroli, N, Nichol, S, Paps, J, Parkinson, J, Pouchkina-Stantcheva, N, Riddiford, N, Rosenzvit, M, Salinas, G, Wasmuth, JD, Zamanian, M, Zheng, Y, The Taenia solium Genome Consortium, Cai, X, Soberón, X, Olson, PD, Laclette, JP, Brehm, K and Berriman, M (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.CrossRefGoogle ScholarPubMed
Voge, M and Seidel, JS (1968) Continuous growth in vitro of Mesocestoides (Cestoda) from oncosphere to fully developed tetrathyridium. The Journal of Parasitology 54, 269.CrossRefGoogle ScholarPubMed
Wagner, DE, Ho, JJ and Reddien, PW (2012) Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10, 299–311.CrossRefGoogle ScholarPubMed
Weick, E-M and Miska, EA (2014) piRNAs: from biogenesis to function. Development 141, 3458–3471.CrossRefGoogle ScholarPubMed
Wickens, M, Bernstein, DS, Kimble, J and Parker, R (2002) A PUF family portrait: 3′UTR regulation as a way of life. Trends in Genetics 18, 150–157.CrossRefGoogle ScholarPubMed
Wikgren, BJP and Gustafsson, MKS (1971) Cell proliferation and histo-genesis in diphyllobothrid tapeworms (Cestoda). Acta Academiae Aboensis. Series B 31, 1–10.Google Scholar
Zeng, A, Li, H, Guo, L, Gao, X, McKinney, S, Wang, Y, Yu, Z, Park, J, Semerad, C, Ross, E, Cheng, L-C, Davies, E, Lei, K, Wang, W, Perera, A, Hall, K, Peak, A, Box, A and Alvarado, AS (2018) Prospectively isolated tetraspanin + neoblasts are adult pluripotent stem cells underlying planaria regeneration. Cell 173, 1593–1608, e20.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Domínguez et al. supplementary material

Figure S1

Download Domínguez et al. supplementary material(Image)
Image 10.3 MB