Ultrastructure of Neoblasts in Turbellarian Geocentrophora wagini Timoshkin, 1984 (Lecithoepitheliata: Plathelminthes)Proceedings of the Zoological Institute RAS, 2016, 320(2): 176–192 · https://doi.org/10.31610/trudyzin/2016.320.2.176 Abstract Acoelomorpha and Plathelminthes have a unique system of stem cells (neoblasts), which is believed to represent a common proliferative compartment of somatic and germ line cells. Meanwhile, on the electron-microscopic level, these cells are not studied in most taxa of Turbellaria. In this study, I describe the ultrastructure of neoblasts in Geocentrophora wagini Timoshkin, 1984 (Lecithoepitheliata, Plathelminthes), an endemic turbellarian from Lake Baikal. The neoblast-like cells showed a high nucleus/cytoplasm ratio. The cytoplasm revealed the features of undifferentiated cells. Particularly, there were free ribosomes and mitochondria, while other organelles were rare and did not occur in all the cells studied. Based on their cytoplasmic and nuclear organization, three main types of parenchymal neoblasts have been distinguished. In type 1, the nuclei had a complex, highly branched configuration. The peripheral heterochromatin was not developed. A large loose structure of fibrous nature and a tiny Golgi apparatus with several secretory granules could be observed in the type 1 neoblast cytoplasm. The nuclei of the type 2 neoblasts had much simpler outlines than those of type 1, despite some processes or invaginations. The poor development of peripheral condensed chromatin was observed and distribution density of the heterochromatin clumps tended to be slightly higher, as compared to type 1. A cluster of small dense granules or a little loose body occasionally could be seen in the proximity to nuclear membrane. Type 3 neoblasts had the most compact nuclei and their heterochromatin was seen as large, irregular clumps of extremely high electron density. Many of these clumps were connected with each other and with the nuclear membrane. The scarce cytoplasm contained only mitochondria and ribosomes. Undifferentiated cells in the gastrodermis were similar to the type 2 neoblasts in the parenchyma. For the first time outside Tricladida special structures were found in the neoblast cytoplasm. These loose fibrous bodies and clusters of granules are likely to be functionally identical to the planarian chromatoid bodies. The obtained results contribute to the comparative morphology of the stem cells in flatworms and basic Bilateria and confirm the heterogeneity of the proliferative compartment in Turbellaria. Key words Lecithoepitheliata, Plathelminthes, stem sells Submitted July 14, 2015 · Accepted March 4, 2016 · Published June 24, 2016 References Aboobaker A.A. 2011. Planarian stem cells: a simple paradigm for regeneration. Trends in Cell Biology, 21(5): 304–11. https://doi.org/10.1016/j.tcb.2011.01.005 Agata K. 2008. Stem Cells in Planarian. In: T.C.G. Bosch (ed.). Stem Cells: From Hydra to Man. Chapter 4. Springer Netherlands, Heidelberg: 59–74. https://doi.org/10.1007/978-1-4020-8274-0_4 Agata K. and Watanabe K. 1999. Molecular and cellular aspects of planarian regeneration. Seminars in Cell and Developmental Biology, 10: 377–383. https://doi.org/10.1006/scdb.1999.0324 Almuedo-Castillo M., Crespo X., Seebeck F., Bartscherer K., Salò E. and Adell T. 2014. JNK Controls the Onset of Mitosis in Planarian Stem Cells and Triggers Apoptotic Cell Death Required for Regeneration and Remodeling. PLoS Genetics, 10(6): e1004400. https://doi.org/10.1371/journal.pgen.1004400 Auladell C., Garcia-Valero J. and Baguñà J. 1993. Ultrastructural localization of RNA in the chromatoid bodies of undifferentiated cells (neoblasts) in planarians by the RNase–gold complex technique. Journal of Morphology, 216(3): 319–326. https://doi.org/10.1002/jmor.1052160307 Baguñà J. 1998. Planarians. In: P. Ferretti and J. Géraudie (eds.). Cellular and Molecular Basis of Regeneration: From Invertebrates to Humans. J. Wiley and Sons, Chichester, New York etc.: 135–165. Baguñà J. 2012. The planarian neoblast: the rambling history of its origin and some current black boxes. The International Journal of Developmental Biology, 56: 19–37. https://doi.org/10.1387/ijdb.113463jb Baguñà J., Salò E. and Auladell C. 1989. Regeneration and pattern formation in planarians III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development, 107: 77–86. https://doi.org/10.1242/dev.107.1.77 Bode A., Salvenmoser W., Nimeth K., Mahlknecht M., Adamski Z., Rieger R.M., Peter R. and Ladurner P. 2006. Immunogold-labeled S-phase neoblasts, total neoblast number, their distribution, and evidence for arrested neoblasts in Macrostomum lignano (Platyhelminthes, Rhabditophora). Cell and Tissue Research, 325: 577–587. https://doi.org/10.1007/s00441-006-0196-2 Coward S.J. 1974. Chromatoid bodies in somatic cells of the planarian: Observations on their behavior during mitosis. The Anatomical Record, 180(3): 533–545. https://doi.org/10.1002/ar.1091800312 De Mulder K., Pfister D., Kuales G., Egger B., Salvenmoser W., Willems M., Steger J., Fauster K., Micura R., Borgonie G. and Ladurner P. 2009. Stem cells are differentially regulated during development, regeneration and homeostasis in flatworms. Developmental Biology, 334(1): 198–212. https://doi.org/10.1016/j.ydbio.2009.07.019 Dimmeler S. and Losordo D. 2011. Stem Cells Review Series: An Introduction. Circulation Research, 109: 907–909. https://doi.org/10.1161/CIRCRESAHA.111.255570 Dirks U., Gruber-Vodicka H.R., Leisch N., Bulgheresi S., Egger B., Ladurner P. and Ott J.A. 2012. Bacterial symbiosis maintenance in the asexually reproducing and regenerating flatworm Paracatenula galateia. PLoS ONE, 7(4): e34709. https://doi.org/10.1371/journal.pone.0034709 Drobysheva I.M. 1983. Autoradiographic study of the digestive parenchyma in Convoluta convoluta (Turbellaria, Acoela). Tsitologiya, 25(11): 1270–1277. [In Russian]. Drobysheva I.M. 1986. Physiological regeneration of the digestive parenchyma in Convoluta convoluta and Oxyposthia praedator (Turbellaria, Acoela). Hydrobiologia, 132: 189–193. https://doi.org/10.1007/BF00046247 Drobysheva I.M. 2007. To the question about tissue arrangement of parenchyma of turbellaria: different types of parenchymal cells in Geocentrophora wagini (Lecithoepitheliata, Plathelminthes). Uchyonye zapiski Kazanskogo gosudarstvennogo universiteta, 149(3): 132–137. [In Russian]. Drobysheva I.M. 2012. Peculiarities of the ultrastructure of stem cells in lecithoepitheliata turbellarian (Plathelminthes). Abstracts of the 24th Russian Conference on Electron Microscopy (29 May–1 June 2012, Chernogolovka). Russian Academy of Sciences, Chernogolovka: 411. [In Russian]. Drobysheva I.M. 2014. Stem cells in turbellarians: variability of ultrastructural features. Proceedings of the II International conference: Modern problems of biological evolution (11–14 March 2014, Moscow). State Darwin Museum, Moscow: 232–235. [In Russian]. Egger B., Steinke D., Tarui H., De Mulder K., Arendt D., Borgonie G., Funayama N., Gschwentner R., Hartenstein V., Hobmayer B., Hooge M., Hrouda M., Ishida S., Kobayashi C., Kuales G., Nishimura O., Pfister D., Rieger R., Salvenmoser W., Smith J., Technau U., Tyler S., Agata K., Salzburger W. and Ladurner P. 2009. To be or not to be a flatworm: The acoel controversy. PLoS ONE, 4(5): e5502. https://doi.org/10.1371/journal.pone.0005502 Ehlers U. 1985. Das Phylogenetische System der Plathelminthes. Gustav Fischer, Stuttgart, New York, 317 p. Eisenhoffer G.T., Kang H. and Sánchez Alvarado A. 2008. Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell, 3(3): 327–339. https://doi.org/10.1016/j.stem.2008.07.002 Elliott S.A. and Sánchez Alvarado A. 2013. The history and enduring contributions of planarians to the study of animal regeneration. Wiley Interdisciplinary Reviews: Developmental Biology, 2(3): 301–326. https://doi.org/10.1002/wdev.82 Fernandéz-Taboada E., Moritz S., Zeuschner D., Stehling M., Schöler H.R., Salό E. and Gentile L. 2010. Development, 137: 1055–1065. https://doi.org/10.1242/dev.042564 Fernández-Taboada E., Rodríguez-Esteban G., Saló E. and Abril J.F. 2011. A proteomics approach to decipher the molecular nature of planarian stem cells. BMC Genomics, 12: 133. https://doi.org/10.1186/1471-2164-12-133 Gentile L., Cebriа F. and Bartscherer K. 2011. The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Disease Models and Mechanisms, 4: 12–19. https://doi.org/10.1242/dmm.006692 González-Estévez C., Felix D.A., Smith M.D., Paps J., Morley S.J., James V., Sharp T.V. and Aboobaker A.A. 2012. SMG-1 and mTORC1 Act Antagonistically to Regulate Response to Injury and Growth in Planarians. PLoS Genetics, 8(3): e1002619. https://doi.org/10.1371/journal.pgen.1002619 Grivennikov I.A. 2008. Embryonic stem cells and the problem of directed differentiation. Uspekhi Biologicheskoi Khimii, 48: 181–220. [In Russian]. Gschwentner R., Ladurner P., Nimeth K. and Rieger R. 2001. Stem cells in a basal bilaterian. S-phase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell and Tissue Research, 304: 401–408. https://doi.org/10.1007/s004410100375 Gustafsson M.K.S. 1977. Aspects of the Cytology and Histogenesis in Cestodes with Special Reference to the Genus Diphyllobothrium. PhD Thesis. Åbo akademi, Åbo, Finland, 73 p. Hayashi T. and Agata K. 2012. A unique FACS method to isolate stem cells in planarian. Methods in Molecular Biology, 879: 29–37. https://doi.org/10.1007/978-1-61779-815-3_2 Hayashi T., Asami M., Higuchi S., Shibata N. and Agata K. 2006. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Development Growth and Differentiation, 48: 371–380. https://doi.org/10.1111/j.1440-169X.2006.00876.x Hayashi T., Shibata N., Okumura R., Kudome T., Nishimura O., Tarui H. and Agata K. 2010. Single-cell gene profiling of planarian stem cells using fluorescent activated cell sorting and its “index sorting” function for stem cell research. Development Growth and Differentiation, 52: 131–144. https://doi.org/10.1111/j.1440-169X.2009.01157.x Hay E.D. and Coward S.J. 1975. Fine structure studies on the planarian, Dugesia: I. Nature of the “neoblast” and other cell types in noninjured worms. Journal of Ultrastructure Research, 50: 1–21. https://doi.org/10.1016/S0022-5320(75)90003-9 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(7): 571–81. https://doi.org/10.1111/j.1440-169X.2007.00947.x Hori I. 1982. An ultrastructural study of the chromatoid body in planarian regenerative cells. Journal of Electron Microscopy, 31(1): 63–72. Hori I. 1992. Cytological approach to morphogenesis in the planarian blastema. I. Cell behavior during blastema formation. Journal of Submicroscopic Cytology and Pathology, 24(1): 75–84. Hori I. 1997. Cytological approach to morphogenesis in the planarian blastema. II. The effect of neuropeptides. Journal of Submicroscopic Cytology and Pathology, 29(1): 91–97. Hori I., Hikosaka-Katayama T. and Kishida Y. 1999. Cytological approach to morphogenesis in the planarian blastema. III. Ultrastructure and regeneration of the acoel turbellarian Convoluta naikaiensis. Journal of Submicroscopic Cytology and Pathology, 31(2): 247–258. Hori I. and Kishida Y. 2003. Quantitative changes in nuclear pores and chromatoid bodies induced by neuropeptides during cell differentiation in the planarian Dugesia japonica. Journal of Submicroscopic Cytology and Pathology, 35(4): 439–44. Korneva Zh.V. 2007. Tissue plasticity and morphogeneses in cestodes. Nauka, Moscow, 187 p. [In Russian]. Ladurner P., Rieger R. and Baguñà J. 2000. Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: A bromodeoxyuridine analysis. Developmental Biology, 226(2): 231–241. https://doi.org/10.1006/dbio.2000.9867 Markosova T.G. and Mamkaev Yu.V. 2000. Morpho-functional investigation of the peripheral parenchyma in Oxyposthia praedator (Acoela). Tsitologiya, 42(8): 740–749. [In Russian]. Moraczewski J. 1977. Asexual reproduction and regeneration of Catenula (Turbellaria, Archoophora). Zoomorphologie, 88: 65–80. https://doi.org/10.1007/BF00993304 Morita M., Best J.B. 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. https://doi.org/10.1016/S0022-5320(69)90017-3 Moritz S., Stöckle F., Ortmeier C., Schmitz H, Rodríguez-Esteban G., Key G. and Gentile L. 2012. Heterogeneity of planarian stem cells in the S/G2/M phase. The International Journal of Developmental Biology, 56: 117–125. https://doi.org/10.1387/ijdb.113440sm Nagamori I. and Sassone-Corsi P. 2008. Spotlight on Germ Cells. The chromatoid body of male germ cells: Epigenetic control and miRNA pathway. Cell Cycle, 7(22): 3503–3508. https://doi.org/10.4161/cc.7.22.6977 Nakagawa H., Ishizu H., Hasegawa R., Kobayashi K. and Matsumoto M. 2012. Drpiwi-1 is essential for germline cell formation during sexualization of the planarian Dugesia ryukyuensis. Developmental Biology, 361: 167–176. https://doi.org/10.1016/j.ydbio.2011.10.014 Newmark P.A., Wang Y. and Chong T. 2008. Germ cell specification and regeneration in planarians. Cold Spring Harbor Symposia on Quantitative Biology, 73: 573–581. https://doi.org/10.1101/sqb.2008.73.022 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. The EMBO Journal, 31(12): 2755–2769. https://doi.org/10.1038/emboj.2012.110 Palmberg I. 1986. Cell migration and differentiation during wound healing and regeneration in Microstomum lineare (Turbellaria). Hydrobiologia, 132: 181–188. https://doi.org/10.1007/BF00046246 Palmberg I. 1990. Stem cells in microturbellarians. An autoradiographic and immunocytochemical study. Protoplasma, 158: 109–120. https://doi.org/10.1007/BF01323123 Palmberg I. 1991. Differentiation during asexual reproduction and regeneration in a microturbellarian. Hydrobiologia, 227: 1–10. https://doi.org/10.1007/BF00027574 Pedersen K.J. 1959. Cytological studies on the planarian neoblast. Zeitschrift für Zellforschung und mikroskopische Anatomie, 50: 799–817. https://doi.org/10.1007/BF00342367 Peter R., Gschwentner R., Schürmann W., Rieger R.M. 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. https://doi.org/10.32725/jab.2004.003 Pfister D., De Mulder K., Hartenstein V., Kuales G., Borgonie G., Marx F., Morris J. and Ladurner P. 2008. Flatworm stem cells and the germ line: Developmental and evolutionary implications of macvasa expression in Macrostomum lignano, 319: 146–159. https://doi.org/10.1016/j.ydbio.2008.02.045 Reddien P.W. 2013. Specialized progenitors and regeneration. Development, 140: 951–957. https://doi.org/10.1242/dev.080499 Reddien P.W. and Sánchez Alvarado A. 2004. Fundamentals of planarian regeneration. Annual Review of Cell and Developmental Biology, 20: 725–757. https://doi.org/10.1146/annurev.cellbio.20.010403.095114 Resch A.M., Palakodeti D., Lu Y.-C., Horowitz M. and Graveley B.R. 2012. Transcriptome Analysis Reveals Strain-Specific and Conserved Stemness Genes in Schmidtea mediterranea. PLoS ONE, 7(4): e34447. https://doi.org/10.1371/journal.pone.0034447 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(2): 127–140. https://doi.org/10.1080/07924259.1999.9652376 Rieger R.M., Tyler S., Smith J.P.S. III and Rieger G.E. 1991. Platyhelminthes: Turbellaria. In: F.M. Harrison and B.J. Bogitsh (Eds.). Microscopic anatomy of invertebrates. V. 3, Platyhelminthes and Nemertinea. Wiley-Liss, New York: 7–140. Rink J.C. 2013. Stem cell systems and regeneration in planaria. Development Genes and Evolution, 223(1–2): 67–84. https://doi.org/10.1007/s00427-012-0426-4 Robb S.M.C., Ross E. and Sánchez Alvarado A. 2008. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Research, 36: D599–D606. https://doi.org/10.1093/nar/gkm684 Robb S.M.C. and Sánchez Alvarado A. 2014. Chapter three – histone modifications and regeneration in the planarian Schmidtea mediterranea. Current Topics in Developmental Biology, 108: 71–93. https://doi.org/10.1016/B978-0-12-391498-9.00004-8 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(1): 16–23. https://doi.org/10.1007/s00018-007-7426-y Rossi L., Salvetti A., Lena A., Batistoni R., Deri P., Pugliesi C., Loreti E. and Gremigni V. 2006. DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Development Genes and Evolution, 216(6): 335–346. https://doi.org/10.1007/s00427-006-0060-0 Rossi L., Salvetti A., Marincola F.M., Lena A., Deri P., Mannini L., Batistoni R., Wang E. and Gremigni V. 2007. Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biology, 8(4): R62. https://doi.org/10.1186/gb-2007-8-4-r62 Rouhana L., Vieira A.P., Roberts-Galbraith R.H. and Newmark P.A., 2012. PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development, 139: 1083–1094. https://doi.org/10.1242/dev.076182 Rouhana L., Weiss J.A., Forsthoefel D.J., Lee H., King R.S., Inoue T., Shibata N., Agata K. and Newmark P.A. 2013. RNA interference by feeding in vitro synthesized doublestranded RNA to planarians: methodology and dynamics. Developmental Dynamics, 242(6): 718–730. https://doi.org/10.1002/dvdy.23950 Rouhana L., Weiss J.A., King R.S. and Newmark P.A. 2014. PIWI homologs mediate Histone H4 mRNA localization to planarian chromatoid bodies. Development, 141(13): 2592–2601. https://doi.org/10.1242/dev.101618 Saló E. 2006. The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays, 28(5): 546–559. https://doi.org/10.1002/bies.20416 Saló E., Abril J.F., Adell T., Cebrià F., Eckelt K., Fernandez-Taboada E., Handberg-Thorsager M., Iglesias M., Molina M.D. and Rodríguez-Esteban G. 2009. Planarian regeneration: achievements and future directions after 20 years of research. The International Journal of Developmental Biology, 53(8–10): 1317–1327. https://doi.org/10.1387/ijdb.072414es Saló E. and Baguñà J. 1984. Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. Journal of Embryology and Experimental Morphology, 83: 63–80. https://doi.org/10.1242/dev.83.1.63 Salvetti A., Rossi L., Bonuccelli L., Lena A., Pugliesi C., Rainaldi G., Evangelista M. and Gremigni V. 2009. Adult stem cell plasticity: Neoblast repopulation in non-lethally irradiated planarians. Developmental Biology, 328: 305–314. https://doi.org/10.1016/j.ydbio.2009.01.029 Sánchez Alvarado A. 2006. Planarian regeneration: Its end is its beginning. Cell, 124: 241–245. https://doi.org/10.1016/j.cell.2006.01.012 Sánchez Alvarado A. 2007. Stem cells and the Planarian Schmidtea mediterranea. C. R. Biologies, 330: 498–503. https://doi.org/10.1016/j.crvi.2007.05.005 Sasidharan V., Lu Y.-Ch., Bansal D., Dasari P., Poduval D., Seshasayee A., Resch A.M., Graveley B.R. and Palakodeti D. 2013. Identification of neoblast- and regeneration-specific miRNAs in the planarian Schmidtea mediterranea. RNA, 19(10): 1394–1404. https://doi.org/10.1261/rna.038653.113 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(9): 615–28. https://doi.org/10.1111/j.1440-169X.2006.00897.x Scimone M.L., Kravarik K.M., Lapan S.W. and Reddien P.W. 2014. Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Reports, 3(2): 339–52. https://doi.org/10.1016/j.stemcr.2014.06.001 Shibata N., Hayashi T., Fukumura R., Fujii J., Kudome-Takamatsu T., Nishimura O., Sano S., Son F., Suzuki N., Araki R., Abe M. and Agata K. 2012. Comprehensive gene expression analyses in pluripotent stem cells of a planarian, Dugesia japonica. The International Journal of Developmental Biology, 56: 93–102. https://doi.org/10.1387/ijdb.113434ns Shibata N., Rouhana L. and Agata K. 2010. Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Development Growth and Differentiation, 52: 27–41. https://doi.org/10.1111/j.1440-169X.2009.01155.x 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(2): 410–421. https://doi.org/10.1016/j.ydbio.2009.01.043 Solana J., Kao D., Mihaylova Y., Jaber-Hijazi F., Malla S., Wilson R. and Aboobaker A. 2012. Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNA-seq, RNA interference and irradiation approach. Genome Biology, 13: R19. https://doi.org/10.1186/gb-2012-13-3-r19 Tasaki J., Shibata N., Nishimura O., Itomi K., Tabata Y., Son F., Suzuki N., Araki R., Abe M., Agata K. and Umesono Y. 2011. ERK signaling controls blastema cell differentiation during planarian regeneration. Development, 138(12): 2417–2427. https://doi.org/10.1242/dev.060764 Vásquez-Doorman C. and Petersen C.P. 2014. zic-1 Expression in Planarian Neoblasts after injury controls anterior pole regeneration. PLoS Genetics, 10(7): e1004452. https://doi.org/10.1371/journal.pgen.1004452 Wagner D.E., Wang I.E. and Reddien P.W. 2011. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science, 332(6031): 811–816. https://doi.org/10.1126/science.1203983 Wagner D.E., Ho J.J. and Reddien P.W. 2012. Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell, 10(3): 299–311. https://doi.org/10.1016/j.stem.2012.01.016 Weissman I.L. 2000. Stem cells: Units of development, units of regeneration, and units in evolution. Cell, 100: 157–168. https://doi.org/10.1016/S0092-8674(00)81692-X 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(12): 3436–3450. https://doi.org/10.1002/dvdy.21375
|
© Zoological Institute of the Russian Academy of Sciences
|