Skip to main content

Stem Cells in Planarian

  • Chapter
Stem Cells

The high regenerative power of planarian has fascinated scientists for a long time. Although many famous scientists, including Thomas Hunt Morgan, extensively devoted themselves to studying mechanisms underlying regeneration, the planarian regeneration still remains mysterious phenomenon. Recently, modern approaches have been developed and incorporated in planarian research, and several mysterious points were clarified. Here, I focus on old problems of planarian stem cells. Planarian stem cells were called “neoblasts” and considered to be the only cells maintaining proliferative activity and pluripotency. However, recent analyses using molecular markers and FACS sorting revealed their heterogeneity. Now we should change the old view of the planarian stem cell system to one closer to mammalian stem cell systems. These insights indicate the planarian regeneration studies may provide new ideas for handling mouse and human ES cells for therapeutic use in the near future.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Agata, K., Watanabe, K. 1999. Molecular and cellular aspects of planarian regeneration. Semin. Cell Dev. Biol. 10: 377–383.

    Article  CAS  PubMed  Google Scholar 

  • Agata, K., Soejima, Y., Kato, K., Kobayashi, C., Umesono, Y., Watanabe, K. 1998. Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zool. Sci. 15: 433–440.

    Article  CAS  PubMed  Google Scholar 

  • Agata, K., Tanaka, T., Kobayashi, C., Kato, K., Saitoh, Y. 2003. Intercalary regeneration in planarians. Dev. Dyn. 226: 308–316.

    Article  CAS  PubMed  Google Scholar 

  • Agata, K., Nakajima, E., Funayama, N., Shibata, N., Saito, Y., Umesono, Y. 2006. Two different evolutionary origins of stem cell systems and their molecular basis. Semin. Cell Dev. Biol. 17: 503–509.

    Article  CAS  PubMed  Google Scholar 

  • Auladell, C., Garicia-Valero, J., Bagunà, J. 1993. Ultrastructural localization of RNA in the chromatoid bodies of undifferentiated cells (neoblasts) in planarians by the RNase-gold complex technique. J. Morphol. 216: 319–326.

    Article  Google Scholar 

  • Baguñà, J. 1981. Planarian neoblasts. Nature 290: 14–15.

    Article  Google Scholar 

  • Baguñà, J., Saló, E., 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.

    Google Scholar 

  • Baguñà, J., Romero, R., Saló, E., Collet, J., Auladell, C., Ribas, M., Riutort, M., García-Fernàndez, J., Burgaya, F., Bueno, D. 1990. Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. Experimental Embryology in Aquatic Plants and Animals. pp. 129–162. Plenum Press, New York.

    Google Scholar 

  • Bradley, A., Evans, M., Kaufman, M.H., Robertson, E. 1984. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309: 255–256.

    Article  CAS  PubMed  Google Scholar 

  • Dubois, F. 1949. Contribution a l’etude de la regeneration chez planaires dulcicoles. Bull. Biol. 83: 213–218.

    Google Scholar 

  • Guo, T., Peters, A.H., Newmark, P.A. 2006. A bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 11: 159–169.

    Article  CAS  PubMed  Google Scholar 

  • Handberg-Thorsager, M., Saló, E. 2007. The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev. Genes Evol. 217: 403–411.

    Article  CAS  PubMed  Google Scholar 

  • Hay, E.D., Coward, S.J. 1975. Fine structure studies on the planarian, Dugesia. I. Nature of the “neoblast” and other cell types in non-injured worms. J. Ultrastruc. Res. 50: 1–21.

    Article  CAS  Google Scholar 

  • Hayashi, T., Asami, M., Higuchi, S., Shibata, N., Agata, K. 2006. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev. Growth Differ. 48: 371–380.

    Article  PubMed  Google Scholar 

  • Higuchi, S., Hayashi, T., Hori, I., Shibata, N., Sakamoto, H., Agata, K. 2007. Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis. Dev. Growth Differ. 49: 571–81.

    PubMed  Google Scholar 

  • Hori, I. 1982. An ultrastructural study of the chromatoid body in planarian regenerative cells. J. Electron Microsc. 31: 63–72.

    Google Scholar 

  • Hori, I. 1992. Cytological approach to morphogenesis in the planarian blastema. 1. Cell behavior during blastema formation. J. Submicrosc. Cytol. Pathol. 24: 75–84.

    Google Scholar 

  • Hori, I. 1997. Cytological approach to morphogenesis in the planarian blastema. II. The effect of neuropeptides. J. Submicrosc. Cytol. Pathol. 29: 91–97.

    CAS  PubMed  Google Scholar 

  • Ito, H., Saito Y., Watanabe K., Orii, H. 2001. Epimorphic regeneration of the distal part of the planarian pharynx. Dev. Genes Evol. 211: 2–9.

    Article  CAS  PubMed  Google Scholar 

  • Kato, K., Orii, H., Watanabe, K., Agata, K. 1999. The role of dorsoventral interaction in the onset of planarian regeneration. Development 126: 1031–1040.

    CAS  PubMed  Google Scholar 

  • Kato, K., Orii, H., Watanabe, K., Agata, K. 2001. Dorsal and ventral position cues residing in differentiated cells are required for the onset of planarian regeneration. Dev. Biol. 233: 109–121.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, K., Arioka, S., Hoshi, M. 2002. Seasonal changes in the sexualization of the planarian Dugesia ryukyuensis. Zool. Sci. 19: 1267–1278.

    Article  PubMed  Google Scholar 

  • Kobayashi, C., Nogi, T., Watanabe, K., Agata, K. 1999. Ectopic pharynx arise by regional reorganization after anterior/posterior grafting in planarians. Mech. Dev. 89: 25–34.

    Article  CAS  PubMed  Google Scholar 

  • Koinuma, S., Umesono, Y., Watanabe, K., Agata, K. 2000. Planaria FoxA (HNF3) homologue is specifically expressed in the pharynx-forming cells. GENE 259: 171–176.

    Article  CAS  PubMed  Google Scholar 

  • Koinuma, S., Umesono, Y., Watanabe, K., Agata, K. 2003. The expression of planarian brain factor homologs, DjFoxG and DjFoxD. Mech. Dev. 3: 21–27.

    CAS  Google Scholar 

  • Mineta, K., Nakazawa, M., Cebrià, F., Ikeo, K., Agata, K., Gojobori, T. 2003. Origin and evolutionary process of the CNS elucidated by comparative genomics analysis of planarian ESTs. Proc. Natl. Acad. Sci. U S A 100: 7666–7671.

    Article  PubMed  Google Scholar 

  • Morgan, T.H. 1898. Experimental studies of the regeneration of Planaria maculata. Arch. Entwicklungsmech. Org. 7: 364–397.

    Article  Google Scholar 

  • National Institutes of Health. 2001. Stem Cells: Scientific Progress and Future Directions. Retrieved 08–05–2004 from http://stemcells.nih.gov/info/basics/.

  • Newmark, P.A., Sánchez Alvarado, A. 2000. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 220: 142–153.

    Article  CAS  PubMed  Google Scholar 

  • Newmark, P.A., Sánchez Alvarado, A. 2002. Not your father’s planarian: a classic model enters the era of functional genomics. Nat. Rev. Genet. 3: 210–219.

    Article  CAS  PubMed  Google Scholar 

  • Orii, H., Miyamoto, T., Agata, K., Watanabe, K. 1995. cDNA cloning and partial sequencing of homeobox genes in Dugesia japonica. Hydrobiologia 305: 277–279.

    Article  CAS  Google Scholar 

  • Orii, H., Kato, K., Agata, K., Watanabe, K. 1998. Molecular cloning of bone morphogenetic protein (BMP) gene from the planarian Dugesia japonica. Zool. Sci. 15: 864–870.

    Article  Google Scholar 

  • Orii, H., Kato, K., Umesono, Y., Agata, K., Watanabe, K. 1999. The planarian HOM/HOX homeobox gene (Plox) expressed along anterior-posterior axis. Dev. Biol. 210: 456–468.

    Article  CAS  PubMed  Google Scholar 

  • Orii, H., Sakurai, T., Watanabe, K. 2005. Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev. Genes Evol. 215: 143–157.

    Article  CAS  PubMed  Google Scholar 

  • Osawa, M., Hanada, K., Hamada, H., Nakauchi, H. 1996. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242–245.

    Article  CAS  PubMed  Google Scholar 

  • Pederson, K.J. 1959. Cytological studies on the planarian neoblast. Z. Zellforsch. 50: 799–817.

    Article  Google Scholar 

  • Randolph, H. 1897. Observations and experiments on regeneration in planarians. Arch. Entw. Mech. Org. 5: 352–372.

    Google Scholar 

  • Reddien, P.W., Oviedo, N.J., Jennings, J.R., Jenkin, J.C., Sánchez Alvarado, A. 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327–1330.

    Article  CAS  PubMed  Google Scholar 

  • Robb, S.M., Ross, E., Sánchez Alvarado, A. 2007. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res. 36: D599–D606.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, L., Salvetti, A., Lena, A., Batistoni, R., Deri, P., Pugliesi, C., Loreti, E., Gremigni, V. 2006. DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev. Genes. Evol. 216: 335–346.

    Article  CAS  PubMed  Google Scholar 

  • Rossi, L., Salvetti, A., Marincola, F.M., Lena, A., Deri, P., Mannini, L., Batistoni, R., Wang, E., Gremigni, V. 2007a. Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biol. 8: R62.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, L., Salvetti, A., Batistoni, R., Deri, P., Gremigni, V. 2007b. Planarians, a tale of stem cells. Cell. Mol. Life Sci. 65: 16–23.

    Article  CAS  Google Scholar 

  • Saito, Y., Koinuma, S., Watanabe, K., Agata, K. 2003. Medio-Lateral intercalation in planarians revealed by grafting experiments. Dev. Dyn. 226: 334–340.

    Article  PubMed  Google Scholar 

  • Salvetti, A., Rossi, L., Lena, A., Batistoni, R., Deri, P., Rainaldi, G., Locci, M.T., Evangelista, M., Gremigni, V. 2005. DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132: 1863–1874.

    Article  CAS  PubMed  Google Scholar 

  • Sánchez Alvarado, A. 2006. Planarian regeneration: its end is its beginning. Cell 124: 241–245.

    Article  PubMed  CAS  Google Scholar 

  • Sánchez Alvarado, A., Newmark, P. 1999. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. U S A 96: 5049–5054.

    Article  PubMed  Google Scholar 

  • Sánchez Alvarado, A., Newmark, P.A., Robb, S.M., Juste, R. 2002. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129: 5659–5665.

    Article  PubMed  CAS  Google Scholar 

  • Sato, K., Shibata, N., Orii, H., Amikura, R., Sakurai, T., Agata, K., Kobayashi, S., Watanabe, K. 2006. Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Dev. Growth Differ. 48: 615–628.

    Article  CAS  PubMed  Google Scholar 

  • Shibata, N., Umesono, Y., Orii, H., Sakurai, T., Watanabe, K, Agata, K. 1999. Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev. Biol. 206: 73–87.

    Article  CAS  PubMed  Google Scholar 

  • Teshirogi, W. 1962. Dynamic morphological change and timetable during the regeneration of the turbellarian. Sci. Rep. Hirosaki Univ. 9: 21–48.

    Google Scholar 

  • Teshirogi, W., Ishida, S. (Eds.) 1987. Biology of Planarians–Foundation, Application & Experiment, Kyoritsu syuppan, Tokyo.

    Google Scholar 

  • Umesono, Y., Watanabe, K., Agata, K. 1997. A planarian orthopedia homolog is specifically expressed in the branch region of both the mature and regenerating brain. Dev. Growth. Differ. 39: 723–727.

    Article  CAS  PubMed  Google Scholar 

  • Umesono, Y., Watanabe, K., Agata, K. 1999. Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev. Genes Evol. 209: 31–39.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Zayas, R.M., Guo, T., Newmark, P.A. 2007. nanos function is essential for development and regeneration of planarian germ cells. Proc. Natl. Acad. Sci. U S A 104: 5901–5906.

    Article  CAS  PubMed  Google Scholar 

  • Wetzel, B.K. 1961. Studies on the fine structure of regenerating Dugesia tigrina. Diss. Harvard Univ. Cambridge, Massachusetts.

    Google Scholar 

  • Wittlieb, J., Khalturin, K., Lohmann, J.U., Anton-Erxleben, F., Bosch, T.C. 2006. Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc. Natl. Acad. Sci. U S A 103: 6208–6211.

    Article  CAS  PubMed  Google Scholar 

  • Wolff, E., Dubois, F. 1948. Sur la migration des cellules de régénération chez les planaires. Rev. Suisse. Zool. 55: 218–227.

    Google Scholar 

  • Yoshida-Kashikawa, M., Shibata, N., Takechi, K., Agata, A. 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. Dev. Dyn. 236: 3436–3450.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science + Business Media B.V

About this chapter

Cite this chapter

Agata, K. (2008). Stem Cells in Planarian. In: Bosch, T.C.G. (eds) Stem Cells. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8274-0_4

Download citation

Publish with us

Policies and ethics