Regeneration in an evolutionarily primitive brain - the planarian Dugesia japonica model

European Journal of Neuroscience

Volumn 34, Issue 6, 2011, Pages 863-869

  Umesono, Yoshihiko ^a,b   Tasaki, Junichi ^a   Nishimura, Kaneyasu ^a,c   Inoue, Takeshi ^a   Agata, Kiyokazu ^a  

^a KYOTO UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Brain regeneration; C Jun N terminal kinase; Cell cycle; Nou darake; Planarian

Indexed keywords

ARTICLE; BEHAVIORAL TRAIT; BIOLOGICAL TRAIT; BRAIN DEVELOPMENT; CELL LINEAGE; CELL REGENERATION; CELL RENEWAL; DUGESIA JAPONICA; DYNAMICS; HOMEOSTASIS; MULTIPOTENT STEM CELL; NEOBLAST; NERVE CELL DIFFERENTIATION; NEUROANATOMY; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGENERATIVE MEDICINE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SOMATIC CELL; TURBELLARIA;

ANIMALS; BRAIN; CELL DIFFERENTIATION; ENVIRONMENT; HOMEOSTASIS; NERVE REGENERATION; PLANARIANS; PLURIPOTENT STEM CELLS;

EID: 80052981801     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07819.x     Document Type: Article

References (65)

1. Agata, K. (2003) Regeneration and gene regulation in planarians. Curr. Opin. Genet. Dev., 13, 492-496.
2. Agata, K. & Umesono, Y. (2008) Brain regeneration from pluripotent stem cells in planarian. Philos. Trans. R. Soc. Lond. B Biol. Sci., 363, 2071-2078.
3. Agata, K. & Watanabe, K. (1999) Molecular and cellular aspects of planarian regeneration. Semin. Cell Dev. Biol., 10, 377-383.
4. 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.
5. Agata, K., Tanaka, T., Kobayashi, C., Kato, K. & Saitoh, Y. (2003) Intercalary regeneration in planarians. Dev. Dyn., 226, 308-316.
6. 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.
7. Agata, K., Saito, Y. & Nakajima, E. (2007) Unifying principles of regeneration I: epimorphosis versus morphallaxis. Dev. Growth Differ., 49, 73-78.
8. Baguñà, J. (1981) Planarian neoblasts. Nature, 290, 14-15.
9. Baguñà, J., Sálo, E. & Auladell, C. (1989) Regeneration and pattern formation in planarians. Evidence that neoblasts are totipotient stem cells and the source of blastema cells. Development, 107, 77-86.
10. Cebrià, F., Kobayashi, C., Umesono, Y., Nakazawa, M., Mineta, K., Ikeo, K., Gojobori, T., Itoh, M., Taira, M., Sánchez Alvarado, A. & Agata, K. (2002a) FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature, 419, 620-624.
11. Cebrià, F., Kudome, T., Nakazawa, M., Mineta, K., Ikeo, K., Gojobori, T. & Agata, K. (2002b) The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mech. Dev., 116, 199-204.
12. Cebrià, F., Nakazawa, M., Mineta, K., Ikeo, K., Gojobori, T. & Agata, K. (2002c) Dissecting planarian central nervous system regeneration by the expression of neural-specific genes. Dev. Growth Differ., 44, 135-146.
13. Evans, M.J. & Kaufman, M.H. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature, 292, 154-156.
14. Fischer, S., Prykhozhij, S., Rau, M. & Neumann, C.J. (2007) Mutation of zebrafish caf-1b results in S phase arrest, defective differentiation and p53-mediated apoptosis during organogenesis. Cell Cycle, 6, 2963-2969.
15. Fraguas, S., Barberán, S. & Cebrià, F. (2011) EGFR signaling regulates cell proliferation, differentiation and morphogenesis during planarian regeneration and homeostasis. Dev. Biol., 354, 87-101.
16. Gurley, K.A., Rink, J.C. & Sánchez Alvarado, A. (2008) Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science, 319, 323-327.
17. 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.
18. Hayashi, T., Shibata, N., Okumura, R., Kudome, T., Nishimura, O., Tarui, H. & 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. Dev. Growth Differ., 52, 131-144.
19. 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, 571-581.
20. Higuchi, S., Hayashi, T., Tarui, H., Nishimura, O., Nishimura, K., Shibata, N., Sakamoto, H. & Agata, K. (2008) Expression and functional analysis of musashi-like genes in planarian CNS regeneration. Mech. Dev., 125, 631-645.
21. Hirth, F., Therianos, S., Loop, T., Gehring, J.W., Reichert, H. & Furukubo Tokunaga, K. (1995) Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron, 15, 769-778.
22. Iglesias, M., Gomez-Skarmeta, J.L., Saló, E. & Adell, T. (2008) Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development, 135, 1215-1221.
23. Inoue, T., Kumamoto, H., Okamoto, K., Umesono, Y., Sakai, M., Sánchez Alvarado, A. & Agata, K. (2004) Morphological and functional recovery of the planarian photosensing system during head regeneration. Zool. Sci., 21, 275-283.
24. Inoue, T., Hayashi, T., Takechi, K. & Agata, K. (2007) Clathrin-mediated endocytic signals are required for the regeneration of, as well as homeostasis in, the planarian CNS. Development, 134, 1679-1689.
25. Kobayashi, C., Kobayashi, S., Orii, H., Watanabe, K. & Agata, K. (1998) Identification of two distinct muscles in the planarian Dugesia japonica by their expression of myosin heavy chain genes. Zool. Sci., 15, 855-863.
26. Kobayashi, C., Saito, Y., Ogawa, K. & Agata, K. (2007) Wnt signaling is required for antero-posterior patterning of the planarian brain. Dev. Biol., 306, 714-724.
27. Martin, G.R. (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA, 78, 7634-7638.
28. McConnell, S.K. & Kaznowski, C.E. (1991) Cell cycle dependence of laminar determination in developing neocortex. Science, 54, 282-285.
29. 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. USA, 100, 7666-7671.
30. Nakazawa, M., Cebrià, F., Mineta, K., Ikeo, K., Agata, K. & Gojobori, T. (2003) Search for the evolutionary origin of a brain: planarian brain characterized by microarray. Mol. Biol. Evol., 20, 784-791.
31. Newmark, P.A. & Sánchez Alvarado, A. (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol., 220, 142-153.
32. Nishimura, K., Kitamura, Y., Inoue, T., Umesono, Y., Sano, S., Yoshimoto, K., Inden, M., Takata, K., Taniguchi, T., Shimohama, S. & Agata, K. (2007a) Reconstruction of dopaminergic neural network and locomotion function in planarian regenerates. Dev. Neurobiol., 67, 1059-1078.
33. Nishimura, K., Kitamura, Y., Inoue, T., Umesono, Y., Yoshimoto, K., Takeuchi, K., Taniguchi, T. & Agata, K. (2007b) Identification and distribution of tryptophan hydroxylase (TPH)-positive neurons in the planarian Dugesia japonica. Neurosci. Res., 59, 101-106.
34. Nishimura, K., Kitamura, Y., Inoue, T., Umesono, Y., Yoshimoto, K., Taniguchi, T. & Agata, K. (2008a) Characterization of tyramine beta-hydroxylase in planarian Dugesia japonica: cloning and expression. Neurochem. Int., 53, 184-192.
35. Nishimura, K., Kitamura, Y., Umesono, Y., Takeuchi, K., Takata, K., Taniguchi, T. & Agata, K. (2008b) Identification of glutamic acid decarboxylase gene and distribution of GABAergic nervous system in the planarian Dugesia japonica. Neuroscience, 153, 1103-1114.
36. Nishimura, K., Kitamura, Y., Taniguchi, T. & Agata, K. (2010) Analysis of motor function modulated by cholinergic neurons in planarian Dugesia japonica. Neuroscience, 168, 18-30.
37. Ogawa, K., Wakayama, A., Kunisada, T., Orii, H., Watanabe, K. & Agata, K. (1998) Identification of a receptor tyrosine kinase involved in germ cell differentiation in planarians. Biochem. Biophys. Res. Commun., 248, 204-209.
38. Ogawa, K., Kobayashi, C., Hayashi, T., Orii, H., Watanabe, K. & Agata, K. (2002) Planarian fibroblast growth factor receptor homologs expressed in stem cells and cephalic ganglions. Dev. Growth Differ., 44, 191-204.
39. Okamoto, K., Takeuchi, K. & Agata, K. (2005) Neural projections in planarian brain revealed by fluorescent dye tracing. Zool. Sci., 22, 535-546.
40. Okano, H., Imai, T. & Okabe, M. (2002) Musashi: a translational regulator of cell fate. J. Cell Sci., 115, 1355-1359.
41. Okano, H., Kawahara, H., Toriya, M., Nakao, K., Shibata, S. & Imai, T. (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp. Cell Res., 306, 349-356.
42. Orii, H., Sakurai, T. & Watanabe, K. (2005) Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev. Genes. Evol., 215, 143-157.
43. Pellettieri, J. & Sánchez Alvarado, A. (2007) Cell turnover and adult tissue homeostasis: from humans to planarians. Annu. Rev. Genet., 41, 83-105.
44. Petersen, C.P. & Reddien, P.W. (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science, 319, 327-330.
45. Pigon, A. (1974) Cephalic mechanisms for social control of fissioning in planarians. II. Localization and identification of the receptors by electron micrographic and ablation studies. J. Neurobiol., 5, 443-462.
46. Pop, R., Shearstone, J.R., Shen, Q., Liu, Y., Hallstrom, K., Koulnis, M., Gribnau, J. & Socolovsky, M. (2010) A key commitment step in erythropoiesis is synchronized with the cell cycle clock through mutual inhibition between PU.1 and S-phase progression. PLoS Biol., 8, e1000484.
47. Rouhana, L., Shibata, N. & Agata, K. (2010) Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance. Dev. Biol., 341, 429-443.
48. Sakai, F., Agata, K., Orii, H. & Watanabe, K. (2000) Organization and regeneration ability of spontaneous supernumerary eyes in planarians-Eye regeneration field and pathway selection by optic nerves. Zool. Sci., 17, 375-381.
49. Sánchez Alvarado, A. & Newmark, P. (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. USA, 96, 5049-5054.
50. Sharif, J., Endoh, M. & Koseki, H. (2011) Epigenetic memory meets G2/M: to remember or to forget? Dev. Cell, 20, 5-6.
51. 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.
52. Shibata, N., Rouhana, L. & Agata, K. (2010) Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Dev. Growth Differ., 52, 27-41.
53. Simeone, A., Acampora, D., Gulisano, M., Stornaiuolo, A. & Boncinelli, E. (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature, 358, 687-690.
54. Takano, T., Pulvers, J.N., Inoue, T., Tarui, H., Sakamoto, H., Agata, K. & Umesono, Y. (2007) Regeneration-dependent conditional gene knockdown (Readyknock) in planarian: demonstration of requirement for Djsnap-25 expression in the brain for negative phototactic behavior. Dev. Growth Differ., 49, 383-394.
55. Tasaki, J., Shibata, N., Nishimura, O., Itomi, K., Tabata, Y., Son, F., Suzuki, N., Araki, R., Abe, M., Agata, K. & Umesono, Y. (2011a) ERK signaling controls blastema cell differentiation during planarian regeneration. Development, 138, 2417-2427.
56. Tasaki, J., Shibata, N., Sakurai, T., Agata, K. & Umesono, Y. (2011b) Role of c-Jun N-terminal kinase activity in blastema formation during planarian regeneration. Dev. Growth Differ., 53, 389-400.
57. Tazaki, A., Gaudieri, S., Ikeo, K., Gojobori, T., Watanabe, K. & Agata, K. (1999) Neural network in planarian revealed by an antibody against planarian synaptotagmin homologue. Biochem. Biophys. Res. Commun., 260, 426-432.
58. Umesono, Y. & Agata, K. (2009) Evolution and regeneration of the planarian central nervous system. Dev. Growth Differ., 51, 185-195.
59. 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.
60. 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.
61. Wagner, D.E., Wang, I.E. & Reddien, P.W. (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science, 332, 811-816.
62. Wolff, E. & Dubois, F. (1948) Suy la migration des celleles de régénération chez les planarians. Rev. Suisse Zool., 55, 218-227.
63. Yazawa, S., Umesono, Y., Hayashi, T., Tarui, H. & Agata, K. (2009) Planarian Hedgehog/Patched establishes anterior-posterior polarity by regulating Wnt signaling. Proc. Natl. Acad. Sci. USA, 106, 22329-22334.
64. Ying, Q.L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P. & Smith, A. (2008) The ground state of embryonic stem cell self-renewal. Nature, 453, 519-523.
65. Yoshida-Kashikawa, M., Shibata, N., Takechi, K. & 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. Dev. Dyn., 236, 3436-3450.