The stem cell system in demosponges: Suggested involvement of two types of cells: Archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells)

Development Genes and Evolution

Volumn 223, Issue 1-2, 2013, Pages 23-38

  Funayama, Noriko ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Archeocytes; Choanocytes; Germ cells; Origin; Stem cells

Indexed keywords

MESSENGER RNA; PIWI PROTEIN; SMALL INTERFERING RNA;

ARCHEOCYTE; ASEXUAL REPRODUCTION; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIFFERENTIATION; CELL DIVISION; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; CELL SIZE; CELL STRUCTURE; CELL SURFACE; CELL TRANSFORMATION; CELL TYPE; CELLULAR DISTRIBUTION; CHOANOCYTE; EFLPIWIA GENE; EFLPIWIB GENE; GAMETE; GENE; GENE EXPRESSION; MEIOSIS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; REVIEW; SPONGE (PORIFERA); STEM CELL; TOTIPOTENT STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; HUMANS; PORIFERA; STEM CELLS;

ANIMALIA; BILATERIA; METAZOA;

EID: 84872947947     PISSN: 0949944X     EISSN: 1432041X     Source Type: Journal    
DOI: 10.1007/s00427-012-0417-5     Document Type: Review

References (112)

1. Adamska M, Degnan BM, Green K, Zwafink C (2011) What sponges can tell us about the evolution of developmental processes. Zool (Jena) 114(1):1-10. doi: 10.1016/j.zool.2010.10.003
2. 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(4):503-509. doi: 10.1016/j.semcdb.2006.05.004 (Pubitemid 44301932)
3. Alie A, Leclere L, Jager M, Dayraud C, Chang P, Le Guyader H, Queinnec E, Manuel M (2011) Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of "germline genes" with stemness. Dev Biol 350(1):183-197. doi: 10.1016/j.ydbio.2010.10.019
4. Anakina RP (1988) The early stages of fertilization of sponge Leucosolenia complicata Montagu (Calcispongia, Leucosoleniida) from the Barents Sea. Porifera and Cnidaria. Modern and perspecitive investigations. Zoological Institute USSR Academy of Science Press, Leningrad
5. Anakina RP, Drozdov AL (2000) Characteristics of oogenesis in the Barents sea sponge Leucosolenia complicata. Tsitologiia 42(2):128-135
6. Anakina RP, Korotkova GP (1989) Spermatogenesis in Leucosolenia complicata Mont., Barents Sea sponge. Ontogenez 20:77-86
7. Borojevic R (1966) Étude expérimentale de la différentiation des cellules de l'éponge au cours de son dévelopement. Dev Biol 14:130-153
8. Borojevic R (1970) Différentiation cellulaire dans l'embryogénèse et la morphogénèse chez les spongiaires. Vol Sym.Zool. Soc. Lond. The Biology of the Porifera. Academic, London
9. Bosch TCG (2008) Stem cells in immortal Hydra. In: Bosch TCG (ed) Stem cells from Hydra to man. Springer, Berlin, pp 37-58
10. Bosch TCG, Anton-Erxleben F, Hemmrich G, Khalturin K (2010) The Hydra polyp: nothing but an active stem cell community. Dev Growth Differ 52:15-25
11. Boury-Esnault N, De Vos L, Donadey C, Vacelet J (1984) Comparative study of the choanosome of Porifera: I. The Homoscleromorpha. J Morphol 180:3-17
12. Boury-Esnault N, Efremova SM, Bézak C, BVacelet J (1999) Reproduction of a hexactinellid sponge: first description of gastrulation by cellular delamination in the Porifera. Invert Rep Dev 35:187-201 (Pubitemid 29407594)
13. Brien P (1973) Les Démosponges, vol 1. Traite de Zoologie, Meison Cie Paris
14. Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton
15. Connes R (1964) Contribution de l'étude de la prolifération par voie asexuée chez le Sycon. Bull Soc Zool France 89:188-195
16. Connes R (1968) Etude histologique, cytologique et expérimentale de la régénération et de la reproduction asexuée chez Tethya lyncurium Lammark (=T. aurantium Pallas (Démosponges)). University, Montpelliar
17. Connes R (1977) Contribution a l'Etude de la gemmulogenése chez la d'Eponge marine Suberites domuncula (Olivi) Nardo. Arch Zool ExpGén 118:391-407
18. Connes R, Paris J, Artiges JM (1974) L'origine des cellules blastogenetiques chez Suberites domuncula Nardo. L'e' quilibre choanocytes-archeocytes chez les spontiaires. Ann Sci Natur Zool (Paris) 16:111-118
19. Custodio MR, Prokic I, Steffen R, Koziol C, Borojevic R, Brummer F, Nickel M, Muller WE (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(1-2):45-59 (Pubitemid 28539180)
20. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K, King N (2011) Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357(1):73-82. doi: 10.1016/j.ydbio.2011.06.003
21. De Goeij JM, De Kluijver A, Van Duyl FC, Vacelet J, Wijffels RH, De Goeij AFPM, Cleutjens JPM, Schutte B (2009) Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding. J Exp Biol 212(23):3892-3900. doi: 10.1242/jeb.034561
22. De Mulder K, Kuales G, Pfister D, Willems M, Egger B, Salvenmoser W, Thaler M, Gorny AK, Hrouda M, Borgonie G, Ladurner P (2009a) Characterization of the stem cell system of the acoel Isodiametra pulchra. BMC Dev Biol 9:69. doi: 10.1186/1471-213X-9-69
23. De Mulder K, Pfister D, Kuales G, Egger B, Salvenmoser W, Willems M, Steger J, Fauster K, Micura R, Borgonie G, Ladurner P (2009b) Stem cells are differentially regulated during development, regeneration and homeostasis in flatworms. Dev Biol 334(1):198-212. doi: 10.1016/j.ydbio.2009.07.019
24. De Sutter D, Buscema M (1977) Isolation of a highly pure archeocytes fraction from the fresh-water sponge Ephydatia fluviatilis. Wilhelm Roux's Archices 183:149-153 (Pubitemid 8205623)
25. 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 Archives Dev Biol 183:151-161 (Pubitemid 8038383)
26. 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(1):99-113
27. Diaz JP (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. Univ. Sci. Tech, Languedoc
28. Diaz JP, Connes R (1980) E' tude ultrastructurale de la spermatogenése d'une démosponge. Biol Cell 38:225-230 (Pubitemid 11200840)
29. Ereskovsky A (2010) The comparative embryology of sponges. Springer, Netherlands
30. Extavour CG (2007) Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr Comp Biol 47(5):770-785. doi: 10.1093/icb/icm027 (Pubitemid 47622330)
31. Fuchs E, Tumbar T, Guasch G (2004) Socializing with the neighbors: stem cells and their niche. Cell 116(6):769-778 (Pubitemid 38410723)
32. Funayama N (2008) Stem cell system of sponge. In: Bosch TCG (ed) Stem cells from Hydra to man. Springer, Berlin, pp 17-35
33. Funayama N (2010) The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev Growth Differ 52(1):1-14. doi: 10.1111/j.1440-169X.2009.01162.x
34. 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(4):243-253 (Pubitemid 40904924)
35. 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. Zoolog Sci 22(10):1113-1122 (Pubitemid 41771732)
36. 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 demosponges. Evol Dev 12(3):275-287
37. 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
38. Gaino E, Burlando B, Buffa P (1986a) Contribution to the study of egg development and derivation in Oscarella lobularis (Porifera, Demospongiae). Int J invert Rep Dev 9:59-69
39. Gaino E, Burlando B, Buffa P, Sará M (1986b) Ultrastructural study of spermatogenesis in Oscarella lobularis (Porifera, Demospongiae). Int J invert Rep Dev 10:297-305
40. Gaino E, Burlando B, Buffa P (1987) Ultrastructural study of oogenesis and fertilization in Sycon ciliatum (Porifera, Calcispongiae). Int J Inv Rep Dev 11:73-82
41. Gallissian MF (1981) Etude ultrastructurale de l'ovogenése chez quelques éponges calcaires (Porifera, Calcarea). Arch Zool Exp Gén 122:329-340
42. Gilis M, Gosselin P, Dubois P, Willenz P (2011) Seasonal modifications and morphogenesis of the hypercalcified sponge Petrobiona massiliana (Calcarea, Calcaronea). Inv Biol 130:193-210
43. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP (2008) Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455(7217):1193-1197. doi: 10.1038/nature07415
44. Gurley KA, Sanchez Alvarado A (2008) Stem cells in animal models of regeneration. In: StemBook. Harvard Stem Cell Institute, Cambridge
45. Haeckel E (1874) Die Gastrae Theorie, die phylogenetische Classfication des Thierreichs und die Homologie der Keimblatter. Jiena Ztscher Natur 8:1-55
46. Höhr D (1977) Differenzierungsvorgänge in der keimenden Gemmula von Ephydatia fluviatilis. Wilhelm Roux's Arch 182:329-346 (Pubitemid 8162572)
47. Ijima I (1901) Studies on the Hexactinelida, contribution I. (Euplectellidae). JColl Sci Imper Univ Tokyo 15:1-299
48. Ishijima J, Iwabe N, Masuda Y, Watanabe Y, Matsuda Y (2008) Sponge cytogenetics - mitotic chromosomes of ten species of freshwater sponge. Zool Sci 25(5):480-486. doi: 10.2108/zsj.25.480
49. Ishizu H, Nagao A, Siomi H (2011) Gatekeepers for Piwi-piRNA complexes to enter the nucleus. Curr Opin Genet Dev 21(4):484-490
50. Ivanova LV (1981) The life cycle of Halichondria panicea (Pallas). Morphogenesis in sponges. Leningrad University Press, Leningrad
51. Juliano C, Wessel G (2010) Developmental biology. Versatile germline genes. Science 329(5992):640-641. doi: 10.1126/science.1194037
52. Juliano C, Wang J, Lin H (2011) Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu Rev Genet 45:447-469
53. Khalturin K, Anton-Erxleben F, Milde S, Plotz C, Wittlieb J, Hemmrich G, Bosch TC (2007) Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Dev Biol 309(1):32-44 (Pubitemid 47302443)
54. King N (2004) The unicellular ancestry of animal development. Dev Cell 7(3):313-325. doi: 10.1016/j.devcel.2004.08.010 (Pubitemid 39236435)
55. King N, Carroll SB (2001) A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. Proc Natl Acad Sci U S A 98(26):15032-15037. doi: 10.1073/pnas.261477698 (Pubitemid 34013964)
56. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451(7180):783-788. doi: 10.1038/nature06617 (Pubitemid 351253174)
57. King N, Young SL, Abedin M, Carr M, Leadbeater BS (2009) The choanoflagellates: heterotrophic nanoflagellates and sister group of the metazoa. Cold Spring Harbor Protoc 2009(2):pdb.emo116. doi: 10.1101/pdb.emo116
58. Korotkova GP (1970) Regeneration and somatic embryogenesis in sponges. The biology of the Porifera. The biology of the Porifera, vol 25. Symposium of the Zoological Society, London
59. Korotkova GP (1997) Regenaration in animals. Petersburg University Press, St. Petersburg
60. Lanna E, Klautau M (2010) Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea). Zoomorphology 129(4):249-261. doi: 10.1007/s00435-010-0117-5
61. Leclere L, Jager M, Barreau C, Chang P, Le Guyader H, Manuel M, Houliston E (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol 364(2):236-248. doi: 10.1016/j.ydbio.2012.01.018
62. Ledger PW, Jones WC (1977) Spicule formation in the calcareous sponge Sycon ciliatum. Cell Tissue Res 181(4):553-567 (Pubitemid 8146823)
63. Lévi C (1970) Les celleles des éponges, vol 25. The biology of the Porifera. Symposium of Zoological Society, London
64. Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Can J Zool 84(2):262-287. doi: 10.1139/z05-170 (Pubitemid 43900035)
65. Leys SP, Mackie GO, Reiswig HM (2007) The biology of glass sponges. Adv Mar Biol 52:1-145. doi: 10.1016/S0065-2881(06)52001-2 (Pubitemid 46217104)
66. Mackie GO, Singla CL (1983) Studies on hexactinellid sponges. 1. Histology of Rhabdocalyptus dawsoni (Lambe, 1873). Philos T Roy Soc B 301(1107):365-400
67. 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(12):591-602
68. 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(6):299-308. doi: 10.1007/s004270100156 (Pubitemid 32821516)
69. 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(10):3024-3039. doi: 10.1002/dvdy.21708
70. Molina MD, Salo E, Cebria F (2009) Expression pattern of the expanded noggin gene family in the planarian Schmidtea mediterranea. Gene Expr Patterns 9(4):246-253
71. Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441(7097):1068-1074. doi: 10.1038/nature04956 (Pubitemid 43990718)
72. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132(4):598-611. doi: 10.1016/j.cell.2008.01.038 (Pubitemid 351253690)
73. Müller WE (2006) The stem cell concept in sponges (Porifera): metazoan traits. Semin Cell Dev Biol 17(4):481-491. doi: 10.1016/j.semcdb.2006. 05.006 (Pubitemid 44301933)
74. Okada Y (1928) On the development of a hexactinellid sponge, Farrea sollasii. J Fac Sci Impr Univ Tokyo 2:1-27
75. Okamoto K, Nakatsukasa M, Alie A, Masuda Y, Agata K, Funayama N (2012) The active stem cell specific expression of sponge Musashi homolog EflMsiA suggests its involvement in maintaining the stem cell state. Mech Dev 129:24-37. doi: 10.1016/j.mod.2012.03.001
76. Palakodeti D, Smielewska M, Lu YC, Yeo GW, Graveley BR (2008) The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14(6):1174-1186. doi: 10.1261/rna.1085008 (Pubitemid 351717497)
77. Paulus W, Weissenfels N (1986) The spermatogenesis of Ephydatia fluviatilis (Porifera). Zoomorphology 106:155-162
78. Pavans de Ceccatty M (1955) Le systéme nerveux des éponges calcaires et siliceuse. Univ, Paris
79. Petersen CP, Reddien PW (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Sci (New York, NY) 319(5861):327-330
80. Philippe H, Roure B (2011) Difficult phylogenetic questions: more data, maybe; better methods, certainly. BMC Biol 9:91. doi: 10.1186/1741-7007-9-91
81. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Worheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Current Biol: CB 19(8):706-712. doi: 10.1016/j.cub.2009.02.052
82. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alie A, Morgenstern B, Manuel M, Worheide G (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27(9):1983-1987. doi: 10.1093/molbev/msq089
83. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sanchez Alvarado A (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Sci (New York, NY) 310(5752):1327-1330. doi: 10.1126/science.1116110 (Pubitemid 41698864)
84. Reddien PW, Bermange AL, Kicza AM, Sanchez Alvarado A (2007) BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134(22):4043-4051 (Pubitemid 350269421)
85. Riesgo A, Maldonado M (2009) Ultrastructure of oogenesis of two oviparous demosponges: Axinella damicornis and Raspaciona aculeata (Porifera). Tissue Cell 41(1):51-65. doi: 10.1016/j.tice.2008.07.004
86. Riesgo A, Maldonado M, Durfort M (2007) Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Mar Fresh Res 58:398-417 (Pubitemid 46639920)
87. 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(6):335-346. doi: 10.1007/s00427-006-0060-0 (Pubitemid 43733123)
88. Rouhana L, Shibata N, Nishimura O, Agata K (2010) Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance. Dev Biol 341(2):429-443. doi: 10.1016/j.ydbio.2010.02.037
89. Rouhana L, Vieira AP, Roberts-Galbraith RH, Newmark PA (2012) PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development 139(6):1083-1094. doi: 10.1242/dev.076182
90. Saller U (1988) Oogenesis and larval development of Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorph 108:23-28
91. Sará M (1955) La nutrizione dell'ovocita in Calcispongie omoceli. Ann Istit Mus Zool Univ Napoli 7:1-30
92. Schulze FE (1875) Uber den bau und Entwicklung von Sycondra raphanus Haeckel. Z Wis Zoll 25:247-280
93. 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):1-7 (Pubitemid 38250214)
94. 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(1):73-87. doi: 10.1006/dbio.1998.9130 (Pubitemid 29069875)
95. Shibata N, Rouhana L, Agata K (2010) Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Dev Growth Differ 52(1):27-41. doi: 10.1111/j.1440-169X.2009.01155.x
96. Shibata N, Hayashi T, Fukumura R, Fujii J, Kudome-Takamatsu T, Nishimura O, Sano S, Son F, Suzuki N, Araki R, Abe M, Agata K (2012) Comprehensive gene expression analyses in pluripotent stem cells of a planarian, Dugesia japonica. Int J Dev Biol 56(1-2-3):93-102. doi: 10.1387/ijdb.113434ns
97. Simpson TL (1984) The cell biology of sponges. Springer, New York
98. Suga H, Sasaki G, Kuma K, Nishiyori H, Hirose N, Su ZH, 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(5):815-818. doi: 10.1016/j.febslet.2008.02.002
99. Sunanaga T, Inubushi H, Kawamura K (2010) Piwi-expressing hemoblasts serve as germline stem cells during postembryonic germ cell specification in colonial ascidian, Botryllus primigenus. Dev Growth Differ 52(7):603-614
100. Takahashi T, Koizumi O, Hayakawa E, Minobe S, Suetsugu R, Kobayakawa Y, Bosch TC, David CN, Fujisawa T (2009) Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra. Dev Genes Evol 219(3):119-129
101. 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 1:561-570
102. Tuzet O (1947) L'ovogenése et la fécondation de l'éponge calcaire Leucosolenia coriacea et de l'éponge siliceuse Reniera elegans. Arch Zool Exp Gén 85:127-148
103. Tuzet O, Paris J (1963) Recherches sur la régéné ration de Sycon raphanus O.S. Vie Milieu 14:285-298
104. 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 AcadSc Paris 270:955-957
105. Tuzet O, Garrone R, Pavans de Ceccatty M (1970b) Obserbations ultrastructurales sur la demosponge Aplysilla rosea Schulze (Dendroceratide): Une metaplasie exemplaire. AnnSciNature Zool Paris 12:27-50
106. Umesono Y, Agata K (2009) Evolution and regeneration of the planarian central nervous system. Dev Growth Differ 51(3):185-195. doi: 10.1111/j.1440-169X.2009.01099.x
107. Vacelet J (1964) Étude monographique de l'éponge calcaire Pharétronide de Méditerranée Petrobiona massiliana Vacelet et Lévi. Les Pharétronides actuelles et fossiles. Rec Trav Stat Mar Endoume 34:1-125
108. Vacelet J (1990) In: Rützler K (ed) New paerspectives in spohge boilogy. Storage cells of calcified relict sponges. Smithsonian Institution Press, Washington DC
109. 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
110. Wilson HV (1907) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5:245-258
111. Witte U, Barthel D (1994) Reproductive cycle and oogenesis of Halichondria panicea (Pallas) in Kiel Bight. Sponges in time and space. Balkema, Rotterdam
112. Yamashita YM (2010) Cell adhesion in regulation of asymmetric stem cell division. Curr Opin Cell Biol 22(5):605-610. doi: 10.1016/j.ceb.2010.07.009