The stem cell system in demosponges: Insights into the origin of somatic stem cells

Development Growth and Differentiation

Volumn 52, Issue 1, 2010, Pages 1-14

  Funayama, Noriko ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Archeocyte; Choanocyte; Pluripotent stem cell; Porifera; Sponge

Indexed keywords

CELL DIFFERENTIATION; CELL RENEWAL; CELL STRUCTURE; CELL TYPE; GAMETE; MOLECULAR EVOLUTION; NONHUMAN; REVIEW; SPONGE (PORIFERA); STEM CELL;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MODELS, BIOLOGICAL; PORIFERA; RNA, SMALL INTERFERING; STEM CELLS;

EPHYDATIA FLUVIATILIS; METAZOA; PORIFERA; SPONGILLIDAE;

EID: 74549137883     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2009.01162.x     Document Type: Review

References (88)

1. Adamska, M., Degnan, S. M., Green, K. M., Adamski, M., Craigie, A., Larroux, C. Degnan, B. M. 2007a. Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2, e1031.
2. Adamska, M., Matus, D. Q., Adamski, M., Green, K., Rokhsar, D. S., Martindale, M. Q. Degnan, B. M. 2007b. The evolutionary origin of hedgehog proteins. Curr. Biol. 17, R836 837.
3. 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.
4. Borojevic, R. 1966. Étude expérimentale de la différentiation des cellules de l'éponge au cours de son dévelopement. Dev. Biol. 14, 130 153.
5. Borojevic, R. 1970. Différentiation cellulaire dans l'embryogénèse et la morphogénèse chez les spongiaires. Academic press, London.
6. Bosch, T. C. G. 2008. Stem cells in immortal hydra. In : Stem Cells From Hydra to Man (ed. T. C. G. Bosch pp. 37 58. Springer, Berlin, Heidelberg.
7. Bosch, T. C. G., Anton-Erxleben, F., Hemmrich, G. Khalturin, K. 2010. The Hydra polyp: nothing but an active stem cell community. Dev. Growth Differ. 52, 15 25.
8. Bosch, T. C. G. David, C. N. 1987. Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev. Biol. 121, 182 191.
9. Boury-Esnault, N. 2006. Systematics and evolution of Demospongiae. Can. J. Zool. 84, 205 224.
10. Brien, P. M. 1932. Contribution a l'etude de la regeneration naturelle chez les spongillidae. Spongilla lacustris (L.), Ephydatia fluviatilis (L.). Arch. Zool. Exp. Gen. 74, 461 506.
11. Brien, P. M. 1976. La croissance des spongillidae. Formation des choanocytes et des spicules. Bull. Biol. France Belg. 110, 211 252.
12. Buss, L. W. 1987. The Evolution of Individuality. Princeton university press, Princeton.
13. Carmell, M. A., Xuan, Z., Zhang, M. Q. Hannon, G. J. 2002. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733 2742.
14. Cerutti, L., Mian, N. Bateman, A. 2000. Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem. Sci. 25, 481 482.
15. Connes, R., Paris, J. Artiges, J. M. 1974. L'origine des cellules blastogenetiques chez Suberites domuncula Nardo. L'équilibre choanocytes-archeocytes chez les spontiaires. Ann. Sci. Natur. Zool. (Paris) 16, 111 118.
16. Custodio, M. R., Prokic, I., Steffen, R., Koziol, C., Borojevic, R., Brummer, F., Nickel, M. Muller, W. E. 1998. Primmorphs generated from dissociated cells of the sponge Suberites domuncula: a model system for studies of cell proliferation and cell death. Mech. Ageing Dev. 105, 45 59.
17. De Sutter, D. Buscema, M. 1977. Isolation of a highly pure archeocyte fraction from the fresh-water sponge Ephydatia fluviatilis. Roux's Arch. Dev. Biol. 183, 149 153.
18. De Sutter, D. Van De Vyver, G. 1977. Aggregative properties of different cell types of the fresh-water sponge Ephydatia fluviatilis isolated on ficoll gradients. Roux's Arch. Dev. Biol. 183, 151 161.
19. Denker, E., Manuel, M., Leclere, L., Le Guyader, H. Rabet, N. 2008. Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev. Biol. 315, 99 113.
20. Diaz, J.-P. 1979. Variations, differenciations et fonctions des categories cellulaire de la demosponge d'eau saumaitres, Suberites massa Nardo, au cours du cycle biologique annuel et dans des conditions experimentales. Thése, pp. 1 332. Univ. Sci. Tech., Languedoc.
21. Diaz, J.-P. Connes, R. 1980. Étude ultrastructurale de la spermatogenése d'une démosponge. Biol. Cell 38, 225 230.
22. Extavour, C. G. M. 2007. Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Int. Comp. Biol. 47, 770 785.
23. Friedlander, M. R., Adamidi, C., Han, T., Lebedeva, S., Isenbarger, T. A., Hirst, M., Marra, M., Nusbaum, C., Lee, W. L., Jenkin, J. C., Alvarado, A. S., Kim, J. K. Rajewsky, N. 2009. High-resolution profiling and discovery of planarian small RNAs. Proc. Natl. Acad. Sci. U S A 106, 11546 11551.
24. Funayama, N. 2008. Stem cell system of sponge. In : Stem Cells From Hydra to Man ed. T. C. G. Bosch pp. 17 35. Springer, Berlin, Heidelberg.
25. Funayama, N., Nakatsukasa, M., Hayashi, T. Agata, K. 2005a. Isolation of the choanocyte in the freshwater sponge, Ephydatia fluviatilis and its lineage marker, Ef annexin. Dev. Growth Differ. 47, 243 253.
26. Funayama, N., Nakatsukasa, M., Kuraku, S., Takechi, K., Dohi, M., Iwabe, N., Miyata, T. Agata, K. 2005b. Isolation of Ef silicatein and Ef lectin as molecular markers for sclerocytes and cells involved in innate immunity in the freshwater sponge, Ephydatia fluviatilis. Zool. Sci. 22, 1113 1122.
27. Funayama, N., Nakatsukasa, M., Mohri, K., Masuda, Y. Agata, K. 2010. Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponge. Evol. Dev. in press.
28. Gaino, E., Burlando, B., Zunino, L., Pansini, M. Buffa, P. 1984. Origin of male gametes from choanocytes in Spongia officinalis (Porifera, Demosongiae). Int. J. Inv. Rep. Dev. 7, 83 93.
29. Garrone, R. Rozenfeld, F. 1981. Electron microscope study of cell differentiation and collagen synthesis in hydroxyurea-treated fresh-water sponges. J. Submicrosc. Cytol. 13, 127 134.
30. Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B. J., Chiang, H. R., King, N., Degnan, B. M., Rokhsar, D. S. Bartel, D. P. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193 1197.
31. Harrison, F. W. 1974. Histology and histochemistry of developing outgrowths of Corvameyenia carolinensis Harrison (Porifera: Spongillidae). J. Morph. 144, 185 194.
32. Hayashi, T., Shibata, N., Okumura, R., Kudome, T., Nishimura, O., Tarui, H. Agata, K. 2010. Single-cell gene profiling of planarian stem cells utilizing FACS and its "index sorting" function for stem cell research. Dev. Growth Differ. in press.
33. Höhr, D. 1977. Differenzierungavorgange in der keimenden gemmula von Ephydatia fluviatilis. Wilhelm Roux's Arch. 182, 329 346.
34. Ishijima, J., Iwabe, N., Masuda, Y., Watanabe, Y. Matsuda, Y. 2008. Sponge cytogenetics - mitotic chromosomes of ten species of freshwater sponge. Zoolog. Sci. 25, 480 486.
35. Khalturin, K., Anton-Erxleben, F., Milde, S., Plotz, C., Wittlieb, J., Hemmrich, G. Bosch, T. C. 2007. Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Dev. Biol. 309, 32 44.
36. King, N. 2004. The unicellular ancestry of animal development. Dev. Cell 7, 313 325.
37. King, N. Carroll, S. B. 2001. A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. Proc. Natl. Acad. Sci. U S A 98, 15032 15037.
38. King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., Marr, M., Pincus, D., Putnam, N., Rokas, A., Wright, K. J., Zuzow, R., Dirks, W., Good, M., Goodstein, D., Lemons, D., Li, W., Lyons, J. B., Morris, A., Nichols, S., Richter, D. J., Salamov, A., Sequencing, J. G., Bork, P., Lim, W. A., Manning, G., Miller, W. T., Mcginnis, W., Shapiro, H., Tjian, R., Grigoriev, I. V. Rokhsar, D. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783 788.
39. Langenbruch, P. F. 1981. Zur entstehung der gemmulae bei Ephydatia fluviatilis L.(Porifera). Zoomorphology 97, 263 284.
40. Leys, S. P. Ereskovsky, A. V. 2006. Embryogenesis and larval differentiation in sponges. Can. J. Zool. 84, 262 287.
41. Leys, S. P., Mackie, G. O. Reiswig, H. M. 2007. The biology of glass sponges. Adv. Mar. Biol. 52, 1 145.
42. Lin, H. Yin, H. 2008. A novel epigenetic mechanism in drosophila somatic cells mediated by Piwi and piRNAs. Cold Spring Harb. Symp. Quant. Biol. 73, 273 281.
43. Mineta, K., Nakazawa, M., Cebria, 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.
44. Mochizuki, K. Gorovsky, M. A. 2004. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev. 18, 2068 2073.
45. Mochizuki, K., Nishimiya-Fujisawa, C. Fujisawa, T. 2001. Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev. Genes. Evol. 211, 299 308.
46. Mochizuki, K., Sano, H., Kobayashi, S., Nishimiya-Fujisawa, C. Fujisawa, T. 2000. Expression and evolutionary conservation of nanos-related genes in Hydra. Dev. Genes. Evol. 210, 591 602.
47. Mohri, K., Nakatsukasa, M., Masuda, Y., Agata, K. Funayama, N. 2008. Toward understanding the morphogenesis of siliceous spicules in freshwater sponge: differential mRNA expression of spicule-type-specific silicatein genes in Ephydatia fluviatilis. Dev. Dyn. 237, 3024 3039.
48. Molina, M. D., Salo, E. Cebria, F. 2009. Expression pattern of the expanded noggin gene family in the planarian Schmidtea mediterranea. Gene Expr. Patterns 9, 246 253.
49. Müller, W. E. 2006. The stem cell concept in sponges (Porifera): Metazoan traits. Semin. Cell Dev. Biol. 17, 481 491.
50. Müller, W. E., Korzhev, M., Le Pennec, G., Müller, I. M. Schröder, H. C. 2003. Origin of metazoan stem cell system in sponges: first approach to establish the model (Suberites domuncula). Biomol. Eng. 20, 369 379.
51. Newmark, P. A., Wang, Y. Chong, T. 2008. Germ cell specification and regeneration in planarians. Cold Spring Harb. Symp. Quant. Biol. 73, 573 581.
52. Palakodeti, D., Smielewska, M., Lu, Y. C., Yeo, G. W. Graveley, B. R. 2008. The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. Rna 14, 1174 1186.
53. Paulus, W. Weissenfels, N. 1986. The spermatogenesis of Ephydatia fluviatilis (Porifera). Zoomorphology 106, 155 162.
54. Perovic, S., Schroder, H. C., Sudek, S., Grebenjuk, V. A., Batel, R., Stifanic, M., Muller, I. M. Muller, W. E. 2003. Expression of one sponge Iroquois homeobox gene in primmorphs from Suberites domuncula during canal formation. Evol. Dev. 5, 240 250.
55. Perovic-Ottstadt, S., Cetkovic, H., Gamulin, V., Schröder, H. C., Kropf, K., Moss, C., Korzhev, M., Diehl-Seifert, B., Müller, I. M. Müller, W. E. 2004. Molecular markers for germ cell differentiation in the demosponge Suberites domuncula. Int. J. Dev. Biol. 48, 293 305.
56. Petersen, C. P. Reddien, P. W. 2008. Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319, 327 330.
57. Rasmont, R. 1975. Freshwater sponges as a material for the study of cell differentiation. Curr. Top. Dev. Biol. 10, 141 159.
58. Reddien, P. W., Bermange, A. L., Kicza, A. M. Sanchez Alvarado, A. 2007. BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134, 4043 4051.
59. Reddien, P. W., Oviedo, N. J., Jennings, J. R., Jenkin, J. C. Sanchez Alvarado, A. 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310, 1327 1330.
60. Richards, G. S., Simionato, E., Perron, M., Adamska, M., Vervoort, M. Degnan, B. M. 2008. Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr. Biol. 18, 1156 1161.
61. 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.
62. Rozenfeld, F. Rasmont, R. 1976. Hydroxyurea: an inhibitor of the differentiation of choanocytes in fresh-water sponges and a possible agent for the isolation of embryonic cells. Differentiation 7, 53 60.
63. Saller, U. 1988. Oogenesis and larval development of Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorphology 108, 23 28.
64. Sanchez Alvarado, A. 2007. Stem cells and the Planarian Schmidtea mediterranea. C. R. Biol. 330, 498 503.
65. Sanchez 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.
66. 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.
67. Schröder, H. C., Krasko, A., Batel, R., Skorokhod, A., Pahler, S., Kruse, M., Müller, I. M. Müller, W. E. 2000. Stimulation of protein (collagen) synthesis in sponge cells by a cardiac myotrophin-related molecule from Suberites domuncula. FASEB J. 14, 2022 2031.
68. Schröder, H. C., Perovic-Ottstadt, S., Wiens, M., Batel, R., Müller, I. M. Müller, W. E. 2004. Differentiation capacity of epithelial cells in the sponge Suberites domuncula. Cell Tissue Res. 316, 271 280.
69. Seipel, K., Yanze, N. Schmid, V. 2004. The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int. J. Dev. Biol. 48, 1 7.
70. Seto, A. G., Kingston, R. E. Lau, N. C. 2007. The coming of age for Piwi proteins. Mol. Cell 26, 603 609.
71. Shibata, N., Rauhana, L. Agata, K. 2010. Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Dev. Growth Differ. 52, 27 41.
72. 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.
73. Simpson, T. L. 1984. The Cell Biology of Sponges. Springer-Verlag, New York Inc.
74. Simpson, T. L. Fell, P. E. 1974. Dormancy among the Porifera: gemmule formatioin and germination in freshwater and marine sponges. Trans. Am. Microsc. Soc. 93, 544 577.
75. Siomi, M. C., Saito, K. Siomi, H. 2008. How selfish retrotransposons are silenced in Drosophila germline and somatic cells. FEBS Lett. 582, 2473 2478.
76. Suga, H., Sasaki, G., Kuma, K., Nishiyori, H., Hirose, N., Su, Z. H., Iwabe, N. Miyata, T. 2008. Ancient divergence of animal protein tyrosine kinase genes demonstrated by a gene family tree including choanoflagellate genes. FEBS Lett. 582, 815 818.
77. Takahashi, T., Koizumi, O., Hayakawa, E., Minobe, S., Suetsugu, R., Kobayakawa, Y., Bosch, T. C., David, C. N. Fujisawa, T. 2009. Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra. Dev. Genes. Evol. 219, 119 129.
78. Tanaka, K. Watanabe, Y. 1984. Choanocyte differentiation and morphogensis of choanocyte chambers in the fresh-water sponge, Ephydatia fluviatilis, after reversal of developmental arrest caused by hydroxyurea. Zool. Sci. 1, 561 540.
79. Tokyocinema, Co., Ltd. 1996. Life of the Freshwater Sponge. TokyoCinema, Co., Ltd, Tokyo.
80. Tuzet, O., Garrone, R. Pavans De Ceccatty, M. 1970a. Origine choancytaire de la lignée germinale mâle chez la démospongie Aplysilla rosea Schulze (Dendroceratide). C. R. Acad.Sc. Paris 270, 955 957.
81. Tuzet, O., Garrone, R. Pavans De Ceccatty, M. 1970b. Obserbations ultrastructurales sur la demosponge Aplysilla rosea Schulze (Dendroceratide): Une metaplasie exemplaire. Ann.Sci.Nat. Zool., Paris 12, 27 50.
82. Umesono, Y. Agata, K. 2009. Evolution and regeneration of the planarian central nervous system. Dev. Growth Differ. 51, 185 195.
83. Unhavaithaya, Y., Hao, Y., Beyret, E., Yin, H., Kuramochi-Miyagawa, S., Nakano, T. Lin, H. 2009. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J. Biol. Chem. 284, 6507 6519.
84. 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.
85. Weissenfels, N. 1975. Bau und Function des Susswasserschwamms Ephydatia fluviatilis L.(Porifera) II. Anmerkungen zum Korperbau. Zeit. Morph. Tiere. 81, 241 256.
86. Weissenfels, N. 1981. Bau und Function des Susswasserschwamms Ephydatia fluviatilis L.(Porifera) VIII.Die Entstehung und Entwicklung der Kragengeibelkammern und ihre Verbindung mit dem ausfuhrenden Kanalsystem. Zoomorphologie 98, 35 45.
87. Wilson, H. V. 1907. On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5, 245 258.
88. Wintermann, G. 1951. Entwicklungsphysiologische Untersuchungen an Süsswasserschwämmen. Zool. Jb. Abt. Anat. Ontog. 71, 427 486.