Skip to main content
SpringerLink
Log in

Stem Cells in Aquatic Invertebrates: Common Premises and Emerging Unique Themes

  • Chapter
  • First Online:
Stem Cells in Marine Organisms

Abstract

The remarkable ability to generate an embryo from a single fertilized oocyte and to regenerate tissues that are injured or going through natural physiological turnover, is the direct result of stem cells, nature’s gift to multicellular organisms. Only recently, studies on marine invertebrates have revealed the diversity of phenomena involved with these cells and their importance to the biology of these organisms. We present an overview on the stem cell biology of four aquatic invertebrate groups: urochordate ascidians, cnidarians, echinoderms and platyhelminthes. While most studies outlined here are based on descriptive data, we found that aquatic invertebrates exhibit multiple cell types with stem cell atributes. Studies revealed that, in contrast to the prevalence of diverse oligopotent and unipotent stem cells in vertebrates, invertebrates appear to display the communal spread of multipotency and pluripotency, with stem cells that give rise to cell lineages characteristic to more than a single germ layer, sometimes with somatic and germ line potentials. The cumulative data further indicate that in contrast to vertebrate systems, stem cells from aquatic invertebrates are disseminated and widespread i.e. not associated with a regulatory microenvironment (niche). We also notice that transdifferentiation is ubiquitous to both anatomically simple and highly evolved invertebrates. These observations delineate common and unique properties to stem cells, posibly tailored, to suit the varied life history and developmental modes characteristic of aquatic invertebrates.

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

Access this chapter

Log in via an institution
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 EPUB and 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

Notes

  1. 1.

    1Reprinted from Vaughn D, Strathmann RR, Predators induce cloning in echinoderm larvae, Fig. 1, p. 1503, (2008), with permission from the America Association for the Advancement of Science.

  2. 2.

    2Reprinted from Vickery et al, Utilization of a novel deuterostome model for the study of regeneration genetics: molecular cloning of genes that are differentially expressed during early stages of larval sea star regeneration, Fig. 1 p 74, (2001a), with permission from Elsevier.

  3. 3.

    3Reprinted from San Miguel-Ruiz and García-Arrarás, Common cellular events occur during wound healing and organ regeneration in the sea cucumber Holothuria glaberrima, Fig. 4 p 6, (2007).

References

  • Abeloos M (1957) Origine de l’organization radiaire dans la régénération des actinies. C R Acad Sci Paris 245:727–729

    CAS  Google Scholar 

  • Abeloos M (1961) Facteurs morphogénétiques dans la régénération des actinies. Ann Fac Sci Marseille 31:11–25

    Google Scholar 

  • Aizu S (1967) Transformation of ectoderm to endoderm in Obelia. Sci Rep Tohoku Univ Ser ΙV (Biol) 33:375–382

    Google Scholar 

  • Aizu S (1968) The role of the interstitial cells on regeneration of new endodermal cells in Coryne. Sci Rep Tohoku Univ Ser ΙV (Biol) 34:91–100

    Google Scholar 

  • Akhmadieva AV, Shukalyuk AI, Aleksandrova YN et al (2007) Stem cells in asexual reproduction of the colonial ascidian Botryllus tubaratus (Tunicata: Ascidiacea). Russ J Mar Biol 33:181–186

    Google Scholar 

  • Alder H, Schmid V (1987) Cell cycles and in vitro transdifferentiation and regeneration of isolated, striated muscle of jellyfish. Dev Biol 124:358–369

    CAS  Google Scholar 

  • Allsopp RC, Chang E, Kashefi-Aazam M, et al (1995) Telomere shortening is associated with cell division in vitro and in vivo. Exp cell Res 220:194–200

    Google Scholar 

  • Alonso L, Fuchs E (2003) Stem cells of the skin epithelium. Proc Natl Acad Sci USA Supp 1:11830–11835

    Google Scholar 

  • Amemiya S, Oji T (1992) Regeneration in sea lilies. Nature 357:546–547

    Google Scholar 

  • Anderson JM (1965) Studies on visceral regeneration in sea-stars. II. Regeneration of pyloric caeca in Asteriidae, with notes on the source of cells in regenerating organs. Biol Bull 128:1–23

    Google Scholar 

  • Angelini C, Amaroli A, Falugi C et al (2003) Acetylcholinesterase activity is affected by stress conditions in Paracentrotus lividus coelomocytes. Mar Biol 143:623–628

    CAS  Google Scholar 

  • Arenas-Mena C, Wong KS-Y, Arandi-Foroshani NR (2007) Histone H2A.Z expression in two indirectly developing marine invertebrates correlates with undifferentiated and multipotent cells. Evol Dev 9:231–243

    CAS  Google Scholar 

  • Baguñà J (1976) Mitosis in the intact and regenerating planarian Dugesia mediterranea n. sp. І Mitotic studies during growth, feeding and starvation. J Exp Zool 195:53–64

    Google Scholar 

  • Baguñà J, Romero R, Saló E et al (1990) Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. In: Marthy HJ (ed) Experimental embryology in aquatic plants and animals. Plenum Press, New York, pp 129–162

    Google Scholar 

  • Baguñà J, Salo 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 206:73–87

    Google Scholar 

  • Baguñà J, Slack JM (1981) Planarian neoblasts. Nature 290:14–15

    Google Scholar 

  • Balser EJ (1998) Cloning by Ophiuroid echinoderm larvae. Biol Bull 194:187–193

    Google Scholar 

  • Bancroft FW (1903) Aestivation of Botrylloides gascoi Della Valle. Mark Anniversary 8:147–166

    Google Scholar 

  • Barth LG (1940) The process of regeneration in Hydroids. Biol Rev 15:405–420

    Google Scholar 

  • Behensky C, Schürmann W (2001) Quantitative analysis of turbellarian cell suspensions by fluorescent staining with acridine orange and video microscopy. Belg J Zool 131:131–136

    Google Scholar 

  • Berrill J (1951) Regeneration and budding in tunicates. Biol Rev 26:456–475

    Google Scholar 

  • Berrill NJ (1941) The Development of the Bud in Botryllus. Biol Bull 80:169–184

    Google Scholar 

  • Betschinger J, Knoblich JA (2004) Dare to be different: Asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr Biol 14:R674–R685

    CAS  Google Scholar 

  • Bickenbach JR (1981) Identification and behavior of label-retaining cells in oral mucosa and skin. J Dent Res 60:1611–1620

    Google Scholar 

  • Bjerknes M, Cheng H (1999) Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 116:7–14

    CAS  Google Scholar 

  • Bode A, Salvenmoser W, Nimeth K et al (2006) Immunogold-labeled S-phase neoblasts, total neoblast number, their distribution, and evidence for arrested neoblasts in Macrostomum lignano (Platyhelminthes, Rhabditophora). Cell Tissue Res 325:577–587

    CAS  Google Scholar 

  • Bode HR (1996) The interstitial cell lineage of Hydra: A stem cell system that arose early in evolution. J Cell Sci 109:1155–1164

    CAS  Google Scholar 

  • Bode HR, Berking S, David CN et al (1973) Quantitative analysis of cell types during growth and morphogenesis in hydra. Wilhelm Roux’s Arch Dev Biol 171:269–285

    Google Scholar 

  • Bode PM, Bode HR (1980) Formation of pattern in regenerating tissue pieces of Hydra attenuata. I. Head-body proportion regulation. Dev Biol 78:484–496

    CAS  Google Scholar 

  • Bosch I, Rivkin RB, Alexander SP (1989) Asexual reproduction by oceanic planktotrophic echinoderm larvae. Nature 337:169–170

    Google Scholar 

  • Bosch TC, David CN (1986) Male and female stem cells and sex reversal in Hydra polyps. Proc Natl Acad Sci USA 83:9478–9482

    CAS  Google Scholar 

  • Bosch TCG (2007) Why polyps regenerate and we don’t: Towards a cellular and molecular framework for Hydra regeneration. Dev Biol 303:421–433

    CAS  Google Scholar 

  • Bosch TCG, David CN (1984) Growth regulation in Hydra: Relationship between epithelial cell cycle length and growth rate. Dev Biol 104:161–170

    CAS  Google Scholar 

  • Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182–191

    Google Scholar 

  • Boyer L, Lee TI, Cole MF et al (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947–956

    CAS  Google Scholar 

  • Brøndsted HV (1942) Further experiments on regeneration-problems in planarians. K Dan Videns Selsk Biol Meddr 17:1–27

    Google Scholar 

  • Brøndsted HV (1969) Planarian regeneration. Pergamon Press, Oxford

    Google Scholar 

  • Brown FD, Swalla BJ (2007) Vasa expression in a colonial ascidian, Botrylloides violaceus. Evol Dev 9:165–177

    CAS  Google Scholar 

  • Bryder D, Rossi DJ, Weissman IL (2006) Hematopoietic stem cells: The paradigmatic tissue-specific stem cell. Am J Pathol 169:338–346

    CAS  Google Scholar 

  • Burighel P, Brunetti R, Zaniolo G (1976) Hibernation of the colonial ascidian Botrylloides leachi (Savigny): Histological observations. Bull Zool 43:293–301

    Google Scholar 

  • Burnett AL, Lowell R, Cyrlin M (1973) Regeneration of a complete Hydra from a single differentiated somatic cell type. In: Burnett AL (ed) Biology of Hydra. Academic Press, New York, pp 225–270

    Google Scholar 

  • Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA 79:5337–5341

    CAS  Google Scholar 

  • Buss LW (1999) Slime molds, ascidians, and the utility of evolutionary theory. Proc Natl Acad Sci USA 96:8801–8803

    CAS  Google Scholar 

  • Cairns J (1975) Mutation selection and the natural history of cancer. Nature 255:197–200

    CAS  Google Scholar 

  • Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 97:4469–4474

    CAS  Google Scholar 

  • Cameron RA, Fraser SE, Britten RJ et al (1991) Macromere cell fates during sea urchin development. Development 113:1085–1091

    CAS  Google Scholar 

  • Campbell RD (1967a) Tissue dynamics of steady state growth in Hydra littoralis. I. Pattern of cell divisions. Dev Biol 15:487–502

    CAS  Google Scholar 

  • Campbell RD (1967b) Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement. J Morphol 121:19–28

    CAS  Google Scholar 

  • Campbell RD, David CN (1974) Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. J Cell Sci 16:349–358

    CAS  Google Scholar 

  • Candelaria AG, Murray G, File SK et al (2006) Contribution of mesenterial muscle dedifferentiation to intestine regeneration in the sea cucumber Holothuria glaberrima. Cell Tissue Res 325:55–65

    Google Scholar 

  • Candia-Carnevali MD, Bonasoro F (1994) Mechanisms of arm regeneration in Antedon mediterranea (Echinodermata, Crinoidea). Anim Biol 9:83–88

    Google Scholar 

  • Candia-Carnevali MD, Bonasoro F (2001) A microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426

    CAS  Google Scholar 

  • Candia-Carnevali MD, Bonasoro F, Biale A (1997) Pattern of bromodeoxyuridine incorporation in the advanced stages of arm regeneration in the feather star Antedon mediterranea. Cell Tissue Res 289:363–374

    CAS  Google Scholar 

  • Candia-Carnevali MD, Bonasoro F, Patruno M et al (1998) Cellular and molecular mechanisms of arm regeneration in crinoid echinoderms: The potential of arm explants. Dev Genes Evol 208:421–430

    CAS  Google Scholar 

  • Candia-Carnevali MD, Bruno L, Donini DS et al (1989) Regeneration and morphogenesis in the feather star arm. In: Kiortsis V, Koussoulakos S, Wallace H (eds) Recent trends in regeneration research. Nano Asi Series, Plenum Press, New York, London, pp 447–460

    Google Scholar 

  • Candia-Carnevali MD, Lucca E, Bonasoro F (1993) Mechanisms of arm regeneration in the feather star Antedon mediterranea: Healing of wound and early stages of development. J Exp Zool 267:299–317

    Google Scholar 

  • Candia-Carnevali MDC (2006) Regeneration in Echinoderms: Repair, regrowth, cloning. Invertebr Surviv J 3:64–76

    Google Scholar 

  • Canicattì C, D’Ancona G (1989) Cellular aspects of Holothuria polii immune response. J Invert Pathol 53:152–158

    Google Scholar 

  • Chandebois R (1976) Histogenesis and morphogenesis in Planarian regeneration. Monogr Dev Biol 11:1–182

    Google Scholar 

  • Child CM (1928) Axial development in aggregates of dissociated cells from Corymorpha. Physiol Zool 1:419–461

    Google Scholar 

  • Cima F, Perin A, Burighel P et al (2001) Morpho-functional characterization of haemocytes of the compound ascidian Botrylloides leachi (Tunicata, Ascidiacea). Acta Zoologica 82:261–274

    Google Scholar 

  • Clevers H (2005) Stem cells, asymmetric division and cancer. Nat Genet 37:1027–1028

    CAS  Google Scholar 

  • Conboy MJ, Karasov AO, Rando TA (2007) High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol 5:E102

    Google Scholar 

  • Consortium SUGS (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952

    Google Scholar 

  • Cotsarelis G, Sun TT, Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: Implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61:1329–1337

    CAS  Google Scholar 

  • Coward SJ (1969) Regeneration in planarians: Some unresolved problems and questions. J Biol Psych 15–19

    Google Scholar 

  • Coward SJ (1974) Chromatoid bodies in somatic cells of the planarian: Observation on their behavior during mitosis. Anat Rec 180:533–546

    CAS  Google Scholar 

  • David CN (1973) A quantitative method for maceration of hydra tissue. Wilhelm Roux’s Arch Dev Biol 171:259–268

    Google Scholar 

  • David CN, Campbell RD (1972) Cell cycle kinetics and development of Hydra attenuata I. Epithelial cells. J Cell Sci 11:557–568

    CAS  Google Scholar 

  • David CN, Murphy S (1977) Characterization of interstitial stem cells in hydra by cloning. Dev Biol 58:372–383

    CAS  Google Scholar 

  • Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: Evolution of developmental regulatory mechanisms. Science 270:1319–1325

    CAS  Google Scholar 

  • Davis LE (1970) Cell division during dedifferentiation and redifferentiation in regenerating isolated gastrodermis of Hydra. Exp Cell Res 60:127–132

    CAS  Google Scholar 

  • Davis LE (1973) Ultrastructural changes during dedifferentiation and redifferentiation in regenerating, isolated gastrodermis. In: Burnett AL (ed) Biology of Hydra. Academic Press New York, London, pp 171–219

    Google Scholar 

  • Delsuc F, Brinkmann H, Chourrout D et al (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968

    CAS  Google Scholar 

  • Diehl FA, Burnett AL (1964) The role of interstitial cells in the maintenance of hydra. I. Specific destruction of interstitial cells in normal, asexual, non-budding animals. J Exp Zool 155:253–260

    CAS  Google Scholar 

  • Dolmatov IY (1992) Regeneration of the aquapharyngeal complex in the holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirota). Monogr Dev Biol 23:40–50

    Google Scholar 

  • Dolmatov IY (1996) Asexual reproduction, evisceration, and regeneration in holothurians. Russ J Dev Biol 27:256–265

    Google Scholar 

  • Drobysheva IM (1986) Physiological regeneration of the digestive parenchyma in Convoluta convoluta and Oxyposthia praedator (Turbellaria, Acoela). Hydrobiologia 132:189–193

    Google Scholar 

  • Drobysheva IM (1988) An autoradiographic study of the replacement of epidermis in polyclad turbellarians. Fortschr Zool 36:97–101

    Google Scholar 

  • Dübel S, Hoffmeister SAH, Schaller HC (1987) Differentiation pathways of ectodermal epithelial cells in hydra. Differentiation 35:181–189

    Google Scholar 

  • Easterday MC, Dougherty JD, Jackson RL et al (2003) Neural progenitor genes. Germinal zone expression and analysis of genetic overlap in stem cell populations. Dev Biol 264:309–322

    CAS  Google Scholar 

  • Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature 425:146

    CAS  Google Scholar 

  • Edds KT (1993) Cell biology of echinoid coelomocytes. I. Diversity and characterization of cell types. J Invert Biol 61:173–178

    Google Scholar 

  • Egger B, Gschwentner R, Rieger R (2007) Free-living flatworms under the knife: Past and present. Dev Genes Evol 217:89–104

    Google Scholar 

  • Egger B, Ladurner P, Nimeth K et al (2006) The regeneration capacity of the flatworm Macrostomum lignano-on repeated regeneration, rejuvenation, and the minimal size needed for regeneration. Dev Genes Evol 216:579–580

    Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: Epigenesis and preformation. Development 130:5869–5884

    CAS  Google Scholar 

  • Faast R, Thonglairoam V, Schulz TC et al (2001) Histone variant H2A.Z is required for early mammalian development. Curr Biol 11:1183–1187

    CAS  Google Scholar 

  • Fischer AB, Hofmann DK, (2004) Budding, bud morphogenesis, and regeneration in Carybdea marsupialis Linnaeus, 1758 (Cnidaria: Cubozoa). Hydrobiologia 530/531:331–337

    Google Scholar 

  • Forsyth NR, Wright WE, Shay JW (2002) Telomerase and differentiation in multicellular organisms: Turn it off, turn it on, turn it off again. Differentiation 69:188–197

    CAS  Google Scholar 

  • Fradkin M, Kakis H, Campbell RD (1978) Effect of gamma irradiation of hydra: Elimination of interstitial cells from viable hydra. Radiat Res 76:187–197

    CAS  Google Scholar 

  • Francis N, Gregg N, Owenb R et al (2006) Lack of age-associated telomere shortening in long- and short-lived species of sea urchins. FEBS Lett 580:4713–4717

    CAS  Google Scholar 

  • Frank U, Leitz T, Müller WA (2001) The hydroid Hydractinia: A versatile, informative cnidarian representative. Bioessays 23:963–971

    CAS  Google Scholar 

  • Freeman G (1964) The role of blood cells in the process of asexual reproduction in the tunicate Perphora viridis. J Exp Zool 156:157–183

    CAS  Google Scholar 

  • Freeman G (1970) The reticuloendothelialystem of tunicates. J Reticuloendothel Soc 7:183–194

    CAS  Google Scholar 

  • Fujiwara S, Kawamura K (1992) Ascidian budding as a transdifferentiation-like system: Multipotent epithelium is not undifferentiated. Dev Growth Differ 34:463–472

    Google Scholar 

  • Fulinski B (1922) Über das Restitutionsvermögen der Rhabdocoelen. Arch Entwm 51:575–586

    Google Scholar 

  • García-Arrarás JE, Estrada-Rodgers L, Santiago R et al (1998) Cellular mechanisms of intestine regeneration in the sea cucumber, Holothuria glaberrima Selenka (Holothuroidea: Echinodermata). J Exp Zool 281:288–304

    Google Scholar 

  • García-Arrarás JE, Greenberg MJ (2001) Visceral regeneration in Holothurians. Microsc Res Tech 55:438–451

    Google Scholar 

  • García-Arrarás JE, Diaz-Miranda L, Torres II et al (1999) Regeneration of the enteric nervous system in the sea cucumber Holothuria glaberrima. J Comp Neurol 406:461–475

    Google Scholar 

  • García-Arrarás JE, Schenk C, Rodrígues-Ramírez R et al (2006) Spherulocytes in the echinoderm Holothuria glaberrima and their involvement in intestinal regeneration. Dev Dyn 235:3259–3267

    Google Scholar 

  • Glinski Z, Jarosz J (2000) Immune phenomena in Echinoderms. Arch Immunol Ther Exp (Warsz) 48:189–193

    CAS  Google Scholar 

  • Gremigni V (1981) The problem of cell totipotency, dedifferentiation and transdifferentiation in Turbellaria. Hydrobiologia 84:171–179

    Google Scholar 

  • Gremigni V, Miceli C, Picano E (1980b) On the role of germ cells in planarian regeneration: ІІ Cytophotometric analysis of the nuclear Feulgen-DNA content in cells of regenerated somatic tissues. J Embryol Exp Morphol 55:65–76

    CAS  Google Scholar 

  • Gremigni V, Miceli C, Puccinelli I (1980a) On the role of germ cells in planarian regeneration: І A karyological investigation. J Embryol Exp Morphol 55:53–63

    CAS  Google Scholar 

  • Gremigni V, Puccinelli I (1977) A contribution to the problem of the origin of blastema cells in planarians: A karyological and ultrastructural investigation. J Exp Zool 199:57–72

    Google Scholar 

  • Gremigni V, Puccinelli I (1979) Sdifferenziamento e migrazione di cellule germinali in planarie tenute a digiuno: Indagine cariologica. Ric Sci Educ Perm Suppl 6:115–116

    Google Scholar 

  • Grimmelikhuijzen CJ, Dockray GJ, Schot LP (1982) FMRFamide-like immunoreactivity in the nervous system of Hydra. Histochemistry 73:499–508

    CAS  Google Scholar 

  • Grosberg RK, Quinn JF (1986) The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322:456–459

    Google Scholar 

  • Gross PS, Al-Sharif WZ, Clow LA et al (1999) Echinoderm immunity and the evolution of the complement system. Dev Comp Immunol 23:429–442

    CAS  Google Scholar 

  • Gross PS, Clow LA, Smith LC (2000) SpC3, the complement homologue from the purple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics 51:1034–1044

    CAS  Google Scholar 

  • Gschwentner R, Ladurner P, Nimeth K et al (2001) Stem cells in a basal bilaterian. Sphase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell Tissue Res 304:401–408

    CAS  Google Scholar 

  • Gustafsson MKS (1976) Studies on cytodifferentiation in the neck region of Diphyllobothrium dendriticum Nitzsch. 1824 (Cestoda, Pseudophyllidae). Z Parasitenk 50:323–329

    CAS  Google Scholar 

  • Hagleithner G (1946) Das Regenerations problem bei Turbellarien. Dissertation, Innsbruck

    Google Scholar 

  • Hammond SM (2006) MicroRNAs as oncogenes. Curr Opin Genet Dev 16:4–9

    CAS  Google Scholar 

  • Hand C, Uhlinger KR (1995) Asexual reproduction by transverse fission and some anomalies in the sea anemone Nematostella vectensis. Invertebr Biol 114:9–18

    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

    CAS  Google Scholar 

  • Haranghy L, Balazs A (1964) Ageing and rejuvenation in planarians. Exp Gerontol 1:77–91

    Google Scholar 

  • Hatfield SD, Shcherbata HR, Fischer KA et al (2005) Stem cell division is regulated by the microRNA pathway. Nature 435:974–978

    CAS  Google Scholar 

  • Hay ED, Coward SJ (1975) Fine structure studies on the planarian Dugesia. Ι Nature of the ‘neoblast’ and other cell types in noninjured worms. J Ultrastruct Res 50:1–21

    CAS  Google Scholar 

  • Hendelberg J, Åkesson B (1991) Studies of the budding process in Convolutriloba retrogemma (Acoela, Platyhelminthes). Hydrobiologia 227:11–17

    Google Scholar 

  • Henson JH, Svitkina TM, Burns AR et al (1999) Two components of actinbased retrograde flow in sea urchin coelomocytes. Mol Biol Cell 10:4075–4090

    CAS  Google Scholar 

  • Higuchi S, Hayashi T, Hori I et al (2007) Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis. Dev Growth Differ 49:571–581

    Google Scholar 

  • Holland ND, Phillips JJH, Giese AC (1965) An autoradiographic investigation of coelomocyte production in the purple sea urchin (Strongylocentrotus purpuratus). Biol Bull 128:259–270

    Google Scholar 

  • Holstein TW, David CN (1990) Cell cycle length, cell size, and proliferation rate in hydra stem cells. Dev Biol 142:392–400

    CAS  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 (1997) Cytological approach to morphogenesis in the planarian blastema. ΙІ. The effect of neuropeptides. J Submicrosc Cytol Pathol 29:91–97

    CAS  Google Scholar 

  • Hyman LH (1955) The Invertebrates Vol 4: Echinodermata. McGraw-Hill, New York, 763p

    Google Scholar 

  • Ivanova NB, Dimos JT, Schanie C et al (2002) A stem cell molecular signature. Science 298:601–604

    CAS  Google Scholar 

  • Izzard CS (1973) Development of polarity and bilateral asymmetry in the palleal bud of Botryllus schlosseri (Pallas) J Morphol 139:1–26

    Google Scholar 

  • Jaeckle WB (1994) Multiple modes of asexual reproduction by tropical and subtropical Sea Star larvae: An unusual adaptation for genet dispersal and survival. Biol Bull 186:62–71

    Google Scholar 

  • Juliano CE, Voronina E, Stack C et al (2006) Germ line determinants are not localized early in sea urchin development, but do accumulate in the small micromere lineage. Dev Biol 300:406–415

    CAS  Google Scholar 

  • Karpowicz P, Morshead C, Kam A et al (2005) Support for the immortal strand hypothesis: Neural stem cells partition DNA asymmetrically in vitro. J Cell Biol 170:721–732

    CAS  Google Scholar 

  • Kawamura K, Fujiwara S (1994) Transdifferentiation of pigmented multipotent epithelium during morphallactic development of budding tunicates. Int J Dev Biol 38:369–377

    CAS  Google Scholar 

  • Kawamura K, Fujiwara S (1995) Cellular and molecular characterization of transdifferentiation in the process of morphallaxis of budding tunicates. Semin Cell Biol 6:117–126

    CAS  Google Scholar 

  • Kawamura K, Nakauchi M (1984) Changes of the atrial epithelium during the development of anteroposterior organization in palleal buds of the polystyelid ascidian, Polyandrocarpa misakiensis. Mem Fac Sci Kochi Univ (Ser D) 5:15–35

    Google Scholar 

  • Kawamura K, Nakauchi M (1986) Development of spatial organization in palleal buds of the compound ascidian, Symplegma reptans. Biol Bull 171:520–537

    Google Scholar 

  • Kawamura K, Nakauchi M (1991b) The effect of aphidicolin on morphogenesis of epithelial stem cells during budding in ascidians. Mem Fac Sci Kochi Univ (Ser D) 12:61–65

    Google Scholar 

  • Kawamura K, Nakauchi N (1991a) Homeostatic integration of stem cell dynamics during palleal budding of ascidians. Zool Sci 8:11–22

    Google Scholar 

  • Kawamura K, Ohkawa S, Michibata H et al (1988) Autoradiographic studies on cell population kinetics in epithelial and haematopoietic stem cell lines in the process of palleal budding of ascidians. Mem Fac Sci Kochi Univ (Ser D) 9:1–12

    Google Scholar 

  • Kiel MJ, He S, Ashkenazi R et al (2007) Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 449:238–242

    CAS  Google Scholar 

  • Knott KE, Balser EJ, Jaeckle WB et al (2003) Identification of Asteroid genera with species capable of larval cloning. Biol Bull 204:246–255

    CAS  Google Scholar 

  • Koguchi S, Sugino YM, Kawamura K (1993) Dynamics of epithelial stem cell in the process of stolonial budding of the colonial ascidian, Perophora japonica. Mem Fac Sci Kochi Univ (Ser D) 14:7–14

    Google Scholar 

  • Koizumi O, Bode HR (1986) Plasticity in the nervous system of adult hydra: I. The position-dependent expression of FMRFamide-like immunoreactivity. Dev Biol 116:407–421

    CAS  Google Scholar 

  • Koizumi O, Bode HR (1991) Plasticity in the nervous system of adult hydra: III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J Neurosci 11:2011–2020

    CAS  Google Scholar 

  • Koizumi O, Heimfeld S, Bode HR (1988) Plasticity in the nervous system of adult hydra: II. Conversion of ganglion cells of the body column into epidermal sensory cells of the hypostome. Dev Biol 129:358–371

    CAS  Google Scholar 

  • Koros AM, Goodwin DG, Siderits RH et al (2002) “Natural killer” (NK) cell antigens CD56, CD57 and others are expressed on breast and lung tumor cells as well as sea urchin coelomocytes. J Biol Regul Homeost Agents 16:173–175

    CAS  Google Scholar 

  • Koros AMC, Pulsford A (1994) Neuroendocrine markers expressed on sea urchin coelomocytes and other immunoregulatory parameters may be used to monitor environmental changes. Ann NY Acad Sci 712:350–353

    CAS  Google Scholar 

  • Kramarsky-Winter E, Loya Y (2000) Tissue regeneration in the coral Fungia granulosa: The effect of extrinsic and intrinsic factors. Mar Biol 137:867–873

    Google Scholar 

  • Lacalli TC (2000) Larval budding, metamorphosis, and the evolution of life-history patterns in echinoderms. Invertebr Biol 119:234–241

    Google Scholar 

  • Ladurner P, Rieger R, Baguñà J (2000) Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine Platyhelminth macrostomum sp.: A bromodeoxyuridine analysis. Dev Biol 226:231–241

    CAS  Google Scholar 

  • Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a colonial ascidian. Cell 123:1351–1360

    CAS  Google Scholar 

  • Laird DJ, Weissman IL (2004) Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate Botryllus schlosseri. Dev Biol 273:185–194

    CAS  Google Scholar 

  • Lang A (1912) Über Regeneration bei Planarien. Arch Mikr Anat 79:361–426

    Google Scholar 

  • Leclerc M, Bajelan M (1992) Homologous antigen for T cell receptor in axial organ cells from the asteroid Asterias rubens. Cell Biol 16:487–490

    CAS  Google Scholar 

  • Leclerc M, Brillouet C, Luquet G (1980) The Starfish axial organ: An ancestral lymphoid organ. Dev Comp Immunol 4:605–615

    CAS  Google Scholar 

  • Lee K, Fajardo MA, Braun RE (1996) A testis cytoplasmic RNA-binding protein that has the properties of a translational repressor. Mol Cell Biol 16:3023–3034

    CAS  Google Scholar 

  • Lender TH, Gabriel A (1965) Les néoblastes marqués par Iuridine tritiée migrent et edifient le blasteme de régénération des planaires d’eau douce. C R Hebd Séanc Acad Sci, Paris 260:4095–4097

    CAS  Google Scholar 

  • Lengner CJ, Camargo FD, Hochedlinger K et al (2007) Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 1:403–415

    CAS  Google Scholar 

  • Lenhoff HM (1965) Cellular segregation and heterocytic dominance in Hydra. Science 148:1105–1107

    CAS  Google Scholar 

  • Lenicque PM, Féral JP (1977) Effects of biogenic amines on the regeneration of small pieces of the pedal disc of the sea anemone Metridium senile (Linnaeus). Comp Biochem Physiol (C Pharmacol Toxicol Endocrinol) 57:91–93

    CAS  Google Scholar 

  • Littlefield CL (1985) Germ cells in Hydra oligactis males. I. Isolation of a subpopulation of interstitial cells that is developmentally restricted to sperm production. Dev Biol 112:185–193

    CAS  Google Scholar 

  • Littlefield CL (1991) Cell lineages in Hydra: Isolation and characterization of an interstitialstem cell restricted to egg production in Hydra oligactis. Dev Biol 143:378–388

    Google Scholar 

  • Magor BG, De Tomaso A, Rinkevich B et al (1999) Allorecognition in colonial tunicates: Protection against predatory cell lineages? Immunol Rev 167:69–79

    CAS  Google Scholar 

  • Manni L, Burighel P (2006) Common and divergent pathways in alternative developmental processes of ascidians. BioEssays 28:902–912

    Google Scholar 

  • Manni L, Zaniolo G, Cima F et al (2007) Botryllus schlosseri: A model ascidian for the study of asexual reproduction. Dev Dyn 236:335–352

    CAS  Google Scholar 

  • Marcum BA, Campbell RD (1978) Developmental roles of epithelial and interstitial cell lineages in hydra: Analysis of chimeras. J Cell Sci 32:233–247

    CAS  Google Scholar 

  • Mashanov VS, Dolmatov IY (2004) Functional morphology of the developing alimentary canal in the holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirota). Acta Zool 85:29–39

    Google Scholar 

  • Mashanov VS, Dolmatov IY, Heinzeller T (2005) Transdifferentiation in holothurian gut regeneration. Biol Bull 209:184–93

    Google Scholar 

  • Matranga V (1996) Molecular aspects of immune reactions in Echinodermata. In: Müller WEG, Rinkevich B (eds) Invertebrate Immunology Vol 15, Progress in Molecular and Subcellular Biology Series. Springer-Verlag, Heidelberg, pp 235–247

    Google Scholar 

  • Matranga V, Bonaventura R, Di Bella G (2002) Hsp70 as a stress marker of sea urchin coelomocytes in short term cultures. Cell Mol Biol 48:345–359

    CAS  Google Scholar 

  • Matranga V, Pinsino A, Celi M et al (2006) Impacts of UV-B radiation on short term cultures of sea urchin coelomocytes. Mar Biol 149:24–34

    Google Scholar 

  • Matranga V, Pinsino A, Celi M et al (2005) Monitoring chemical and physical stress using sea urchin immune cells. Prog Mol Subcell Biol 39:85–110

    CAS  Google Scholar 

  • Matranga V, Toia G, Bonaventura R et al (2000) Cellular and biochemical responses to environmental and experimentally induced stress in sea urchin coelomocytes. Cell Stress Chaperones 5:158–165

    Google Scholar 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  Google Scholar 

  • Metcalf D, Moore MAS (1971) Hematopoietic cells. North Holland Publishing Co., Amsterdam, pp 235–247

    Google Scholar 

  • Millott N (1969) Injury and the axial organ of echinoids. Experientia 25:756

    Google Scholar 

  • Mladenov PV, Bisgrove B, Asotra S et al (1989) Mechanisms of arm-tip regeneration in the sea star, Leptasterias hexactis. Roux’s Arch Dev Biol 189:19–28

    Google Scholar 

  • Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T (2001) Universal occurrence of the vasa-related genes among meta-zoans and their germline expression in Hydra. Dev Genes Evol 211:299–308

    CAS  Google Scholar 

  • Mochizuki K, Sano H, Kobayashi S et al (2000) Expression and evolutionary conservation of nanos-related genes in Hydra. Dev Genes Evol 210:591–602

    CAS  Google Scholar 

  • Montgomery JR, Coward SJ (1974) On the minimal size of a planarian capable of regeneration. Trans Am Microsc Soc 93:386–391

    CAS  Google Scholar 

  • Moore KA, Lemischka IR (2006) Stem cells and their niches. Science 311:1880–1885

    CAS  Google Scholar 

  • Morgan TH (1902) Growth and regeneration in Planaria lugubris. Arch Entwm 13:179–212

    Google Scholar 

  • Morita M (1995) Structure and function of the reticular cell in the planarian Dugesia dorotocephala. Hydrobiologia 305:189–196

    Google Scholar 

  • Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441:1068–1074

    CAS  Google Scholar 

  • Morrison SJ, Prowse KR, Ho P et al (1996) Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity 5:207–216

    CAS  Google Scholar 

  • Mortensen T (1921) Studies of the Development and Larval Form of Echinoderms. GEC Gad, Copenhagen 266p

    Google Scholar 

  • Moss C, Hunter J, Thorndyke MC (1998) Pattern of bromodeoxyuridine incorporation and neuropeptide immunoreactivity during arm regeneration in the starfish Asterias rubens. Philos Trans R Soc Lond B 353:421–436

    CAS  Google Scholar 

  • Mukai H, Koyama H, Watanabe H (1983) Studies on the reproduction of three species of Perophora (Ascidianea). Biol Bull 164:251–266

    Google Scholar 

  • Müller WA, Plickert G, Berking S (1986) Regeneration in Hydrozoa: Distal versus proximal transformation in Hydractinia. Dev Genes Evol 195:513–518

    Google Scholar 

  • Müller WA, Teo R, Frank U (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275:215–224

    Google Scholar 

  • Munoz-Chapuli R, Carmona R, Guadix JA et al (2005) The origin of the endothelial cells: An evo-devo approach for the invertebrate/vertebrate transition of the circulatory system. Evol Dev 7:351–358

    CAS  Google Scholar 

  • Murray G, García-Arrarás JE (2004) Myogenesis during holothurian intestinal regeneration. Cell Tissue Res 318:515–524

    Google Scholar 

  • Nakauchi M (1982) Asexual development of ascidians: Its biological significance, diversity, and morphogenesis. Am Zool 22:753–763

    Google Scholar 

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

    CAS  Google Scholar 

  • Nimeth KT, Mahlknecht M, Mezzanato A et al (2004) Stem cell dynamics during growth, feeding, and starvation in the basal flatworm Macrostomum sp. (Platyhelminthes). Dev Dyn 230:91–99

    Google Scholar 

  • Nishimiya-Fujisawa C, Sugiyama T (1993) Genetic analysis of developmental mechanisms in hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata. Dev Biol 157:1–9

    CAS  Google Scholar 

  • Nishimiya-Fujisawa C, Sugiyama T (1995) Genetic analysis of developmental mechanisms in Hydra. XXII. Two types of female germ stem cells are present in a male strain of Hydra magnipapillata. Dev Biol 172324–336

    Google Scholar 

  • Nunzi MG, Burighel P, Schiaffino S (1979) Muscle cell differentiation in the ascidian heart. Dev Biol 68:371–380

    CAS  Google Scholar 

  • Oka H, Watanabe H (1957a) Vascular budding, a new type of budding in Botryllus. Biol Bull 112:225–240

    Google Scholar 

  • Oka H, Watanabe H (1957b) Colony specificity in compound ascidians as tested by fusion experiments. Proc Japan Acad 33:627–659

    Google Scholar 

  • Oka H, Watanabe H (1959) Vascular budding in Botrylloides. Biol Bull 117:340–346

    Google Scholar 

  • Oren U, Rinkevich B, Loya Y (1997) Oriented intra-colonial transport of 14C labeled materials during coral regeneration. Mar Ecol Prog Ser 161:117–122

    Google Scholar 

  • Oweson C, Sköld H, Pinsino A et al (2008) Manganese effects on haematopoietic cells and circulating coelomocytes of Asterias rubens (Linnaeus). Aquat Toxicol 89:75–81

    Google Scholar 

  • Palmberg I (1986) Cell migration and differentiation during wound healing and regeneration in Microstomum lineare (Turbellaria). Hydrobiologia 132:181–188

    Google Scholar 

  • Palmberg I (1990) Stem cells in microturbellarians-an autoradiographic and immunocytochemical study. Protoplasma 158:109–120

    Google Scholar 

  • Palmberg I, Reuter M (1983) Asexual reproduktion in Microstomum lineare (Turbellaria). I. An autoradiographic and ultrastructural study. Int J Invert Reprod 6:197–206

    Google Scholar 

  • Pancer Z, Gershon H, Rinkevich B (1995) Cloning of a urochordate cDNA featuring mammalian short consensus repeats (SCR) of complement-control protein superfamily. Comp Biochem Physiol B Biochem Mol Biol 111:625–632

    CAS  Google Scholar 

  • Pedersen KJ (1972) Studies on regeneration blastemas of the planarian Dugesia tigrina with special reference to differentiation of the muscle-connective tissue filament system. Wilhelm Roux Arch Entw Mech 169:134–169

    Google Scholar 

  • Peterson KJ, Cameron RA, Davidson EH (1997) Set-aside cells in maximal indirect development: Evolutionary and developmental significance. BioEssays 19:623–631

    CAS  Google Scholar 

  • Peterson KJ, Cameron RA, Davidson EH (2000) Bilaterian origins: Significance of new experimental observations. Dev Biol 219:1–17

    CAS  Google Scholar 

  • Pinsino A, Della Torre C, Sammarini V et al (2008) Sea urchin coelomocytes as a novel cellular biosensor of environmental stress: A field study in the Tremiti Island Marine Protected Area Southern Adriatic Sea, Italy. Cell Biol Toxicol Epub 24:541–52

    Google Scholar 

  • Pinsino A, Thorndyke MC, Matranga V (2007) Coelomocytes and post-traumatic response in the common sea star Asterias rubens Cell Stress Chaperones 12:332–342

    Google Scholar 

  • Polteva DG, Lenicque PM (1970) Effets des neuromédiateurs sur lémbryogénèse somatique chez Meteridium senile. Thérapie 25:1067–1081

    CAS  Google Scholar 

  • Potten CS, Hume WJ, Reid P et al (1978) The segregation of DNA in epithelial stem cells. Cell 15:899–906

    CAS  Google Scholar 

  • Potten CS, Owen G, Booth D (2002) Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 115:2381–2388

    CAS  Google Scholar 

  • Pyle AD, Donovan PJ, Lock LF (2004) Chipping away at ‘stemness’. Genome Biol 5:235

    Google Scholar 

  • Raftos DA, Cooper EL (1991) Proliferation of lymphocyte-like cells from the solitary tunicate, Styela clava, in response to allogeneic stimuli. J Exp Zool 260:391–400

    CAS  Google Scholar 

  • Ramalho-Santos M, Yoon S, Matsuzaki Y et al (2002) “Stemness”: Transcriptional profiling of embryonic and adult stem cells. Science 298:597–600

    CAS  Google Scholar 

  • Rando TA (2007) The immortal strand hypothesis: Segregation and reconstruction. Cell 129:1239–1243

    CAS  Google Scholar 

  • Ransick A, Cameron RA, Davidson EH (1996) Postembryonic segregation of the germ line in sea urchins in relation to indirect development. Proc Natl Acad Sci USA 93:6759–6763

    CAS  Google Scholar 

  • Reber-Müller S, Ono S, Shimizu O et al (1994) Transdifferentiation of striated muscle of jellyfish to smooth muscle and nerve cells: The role of cell-ECM interactions and carbohydrates revealed by a monoclonal antibody. Differentiation 57:77–87

    Google Scholar 

  • Reddien PW, Oviedo NJ, Jennings JR et al (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310:1327–1330

    CAS  Google Scholar 

  • Reiger R (1986) Asexual reproduction and the turbellarian archetype. Hydrobiologia 132:35–45

    Google Scholar 

  • Reuter M, Kreshchenko N (2004) Flatworm asexual multiplication implicates stem cells and regeneration. Can J Zool 82:334–356

    Google Scholar 

  • Rieger RM, Legniti A, Ladurner P et al (1999) Ultrastructure of neoblasts in microturbellaria: Significance for understanding stem cells in free-living Platyhelminthes. Invertebr Reprod Dev 35:127–140

    Google Scholar 

  • Rinkevich B (2002a) The colonial urochordate Botryllus schlosseri: From stem cells and natural tissue transplantation to issues in evolutionary ecology. Bio Essays 24:730–740

    Google Scholar 

  • Rinkevich B (2002b) Germ cell parasitism as an ecological and evolutionary puzzle: Hitchhiking with positively selected genotypes. OIKOS 96:25–30

    Google Scholar 

  • Rinkevich B, Shapira M (1999) Multi-partner urochordate chimeras outperform two-partner chimerical entities. OIKOS 87:315–320

    Google Scholar 

  • Rinkevich B, Shlemberg Z, Fishelson L (1995) Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci USA 92:7695–7699

    CAS  Google Scholar 

  • Rinkevich B, Shlemberg Z, Fishelson L (1996) Survival budding processes in the colonial tunicate Botrylloides from the Mediterranean Sea: The role of totipotent blood cells. In: Maramorosch K, Loeb MJ, Largo MD (eds) Invertebrate cell culture: Looking towards the 21st century. Society for In Vitro Biology, Raleigh, pp 1–9

    Google Scholar 

  • Rinkevich B, Weissman IL (1987a) Chimeras in colonial invertebrates: A synergistic symbiosis or somatic-and germ-cell parasitism. Symbiosis 4:117–134

    Google Scholar 

  • Rinkevich B, Weissman IL (1987b) A long-term study on fused subclones in the ascidian Botryllus schlosseri: The resorption phenomenon (Protochordata: Tunicata). J Zool Lond 213:717–733

    Google Scholar 

  • Rinkevich B, Weissman IL (1992) Chimeras vs genetically homogeneous individuals: Potential fitness costs and benefits. OIKOS 63:119–124

    Google Scholar 

  • Rinkevich B, Weissman IL, De Tomaso AW (1998) Transplantation of Fu/HC-incompatible zooids in Botryllus schlosseri results in chimerism. Biol Bull 195:98–106

    CAS  Google Scholar 

  • Rinkevich B, Yankelevich I (2004) Environmental split between germ cell parasitism and somatic cell synergism in chimeras of a colonial urochordate. J Exp Biol 207:3531–3536

    Google Scholar 

  • Rinkevich Y, Paz G, Rinkevich B et al (2007) Systemic bud iduction and retinoic acid signaling underlie whole body rgeneration in the urochordate Botrylloides leachi. PLoS Biol 5:900–913

    CAS  Google Scholar 

  • Rodriguez AJ, Seipel SA, Hamill DR et al (2005) Seawi, a sea urchin piwi/argonaute family member is a component of MT-RNP complexes. RNA 11:656–656

    Google Scholar 

  • Rosner A, Paz G, Rinkevich B (2006) Divergent roles of the DEAD-box protein BSPL10, the urochordate homologue of human DDX3 and DDX3Y proteins, in colony astogeny and ontogeny. Dev Dyn 235:1508–1521

    CAS  Google Scholar 

  • Rossi L, Salvetti A, Lena A et al (2006) DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev Genes Evol 216:335–346

    CAS  Google Scholar 

  • Sabbadin A (1955) Studies on blood cells in Botryllus schlosseri (Pallas). Arch Ital Anat Istol Patol 60:33–67

    CAS  Google Scholar 

  • Sabbadin A (1962) La basi genetiche della capacita di fusione fra colonie in Botryllus schlosseri (Ascidiacea). Rend Accad Lincei 32:1031–1035

    Google Scholar 

  • Sabbadin A, Astorri C (1988) Chimeras and histocompatibility in the colonial ascidian Botryllus schlosseri. Dev Comp Immunol 12:737–747

    CAS  Google Scholar 

  • Sabbadin A, Zaniolo G (1979) Sexual differentiseriation and germ cell transfer in the colonial ascidian Botryllus schlosseri. J Exp Zool 207:289–304

    Google Scholar 

  • Sacks PG, Davis LE (1979) Production of nerveless Hydra attenuata by hydroxyurea treatments. J Cell Sci 37:189–203

    CAS  Google Scholar 

  • Saló E, Aguñà 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. J Embryol Exp Morphol 83:63–80

    Google Scholar 

  • Sánchez-Alvarado A (2000) Regeneration in the metazoans: Why does it happen? BioEssays 22:578–590

    Google Scholar 

  • San Miguel-Ruiz JE, García-Arrarás JE (2007) Common cellular events occur during wound healing and organ regeneration in the sea cucumber Holothuria glaberrima. BMC Dev Biol 7:115

    Google Scholar 

  • Sato K, Shibata N, Orii H et al (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

    CAS  Google Scholar 

  • Sato N, Sanjuan IM, Heke M et al (2003) Molecular signature of human embryonic stem cells and its comparison with the mouse. Dev Biol 260:404–413

    CAS  Google Scholar 

  • Satoh N, Levine M (2005) Surfing with the tunicates into the post-genome era. Genes Dev 19:2407–2411

    CAS  Google Scholar 

  • Schmid V, Alder H (1984) Isolated, mononucleated, striated muscle can undergo pluripotent transdifferentiation and form a complex regenerate. Cell 38:801–809

    CAS  Google Scholar 

  • Schürmann W, Betz S (1998) Separation and subtyping of planarian neoblasts by densitygradient centrifugation and staining. Hydrobiologia 383:117–124

    Google Scholar 

  • Scofield VL, Schlumpberger JM, West LA et al (1982) Protochordate allorecognition is controlled by an MHC-like gene system. Nature 295:499–502

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Sharpless NE, DePinho RA (2004) Telomeres, stem cells, senescence, and cancer. J Clin Invest 113:160–168

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Shimizu H, Sawada Y, Sugiyama T (1993) Minimum tissue size required for hydra regeneration. Dev Biol 155:287–296

    CAS  Google Scholar 

  • Shinin V, Gayraud-Morel B, Gomès D et al (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8:677–687

    CAS  Google Scholar 

  • Siebert S, Anton-Erxleben F, Bosch TC (2008) Cell type complexity in the basal metazoan Hydra is maintained by both stem cell based mechanisms and transdifferentiation. Dev Biol 313:13–24

    CAS  Google Scholar 

  • Siffroi JP, Pawlak A, Alfonsi MF et al (2001) Expression of the TAR RNA binding protein in human testis. Mol Hum Reprod 7:219–225

    CAS  Google Scholar 

  • Simon-Blecher N, Achituv Y, Rinkevich B (2004) Protochordate concordant xenotransplantation settings reveal outbreaks of donor cells and divergent life span traits. Dev Comp Immunol 28:983–991

    CAS  Google Scholar 

  • Smid I, Tardent P (1986) The potentialities of endoderm interstitial cells in Hydra attenuata Pall. Dev Biol 117:672–675

    Google Scholar 

  • Smith GH (2005) Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 132:681–687

    CAS  Google Scholar 

  • Smith LC, Rast JP, Brockton V et al (2006) The sea urchin immune system. Invertebr Surviv J 3:25–39

    Google Scholar 

  • Smith VJ (1981) The echinoderms. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells. Academic Press, New York, pp 513–562

    Google Scholar 

  • Song JL, Wessel GM (2007) Genes involved in the RNA interference pathway are differentially expressed during sea urchin development. Dev Dyn 236:3180–3190

    CAS  Google Scholar 

  • Spradling A, Drummond-Barbosa D, Kai T (2001) Stem cells find their niche. Nature 414:98–104

    CAS  Google Scholar 

  • Steinberg MS (1963) The regeneration of whole polyps from ectodermal fragments of scyphostoma larvae of Aurelia aurata. Biol Bull 114:337–343

    Google Scholar 

  • Steinmann P (1925) Das verhalten der Zellen und Gewebe im regenerienden Tricladen Körper. Verh Naturforsch Ges 36:133–162

    Google Scholar 

  • Stoner DS, Rinkevich B, Weissman IL (1999) Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. Proc Natl Acad Sci USA 96:9148–9153

    CAS  Google Scholar 

  • Stoner DS, Weissman IL (1996) Somatic and germ cell parasitism in a colonial ascidian: Possible role for a highly polymorphic allorecognition system. Proc Natl Acad Sci USA 93:15254–15259

    CAS  Google Scholar 

  • Sugiyama T, Fujisawa T (1978) Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. J Cell Sci 29:35–52

    CAS  Google Scholar 

  • Sunanaga T, Saito Y, Kawamura K (2006) Postembryonic epigenesis of Vasa-positive germ cells from aggregated hemoblasts in the colonial ascidian, Botryllus primigenus. Dev Growth Differ 48:87–100

    Google Scholar 

  • Sunanaga T, Watanabe A, Kawamura K (2007) Involvement of vasa homolog in germline recruitment from coelomic stem cells in budding tunicates. Dev Genes Evol 217:1–11

    Google Scholar 

  • Sutton MF (1953) The regeneration of the siphons of Ciona intestinalis L. J Mar Biol Assc UK 32:249–268

    Google Scholar 

  • Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872

    CAS  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    CAS  Google Scholar 

  • Taneda Y, Watanabe H (1982) Effects of X-irradiation on colony specificity in the compound ascidian, Botryllus primigenus Oka. Dev Comp Immunol 6:665–673

    CAS  Google Scholar 

  • Terada H, Sugiyama T, Shigenaka Y (1988) Genetic analysis of developmental mechanisms in hydra. XVIII. Mechanism for elimination of the interstitial cell lineage in the mutant strain Sf-1. Dev Biol 126:263–269

    CAS  Google Scholar 

  • Teshirogi W (1967) Heteroplastic transplantation in the freshwater planarians Bdellocephala brunnea and Dendrocoelopsis lacteus. Sci Rep Tohoku Univ Ser ΙV (Biol) 33:383–397

    Google Scholar 

  • Thouveny Y, Tassava RA (1998) Regeneration through phylogenesis. In: Ferretti P, Geraudie J (eds) Cellular and molecular basis of regeneration: From invertebrates to humans. John Wiley & Sons Ltd, Chichester, UK, pp 9–43

    Google Scholar 

  • Till JE, McCulloch EA (1961) Direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14:213–222

    CAS  Google Scholar 

  • Tiozzo S, Christiaen L, Deyts C et al (2005) Embryonic versus blastogenetic development in the compound ascidian Botryllus schlosseri: Insights from Pitx expression patterns. Dev Dyn 232:468–478

    CAS  Google Scholar 

  • Tiozzo S, Voskoboynik A, Brown FD et al (2008) A conserved role of the VEGF pathway in angiogenesis of an ectodermally-derived vasculature. Dev Biol 315:243–255

    CAS  Google Scholar 

  • Toledo A, Cruz C, Fragoso G et al (1997) In vitro culture of Taenia crassiceps larval cells and cyst regeneration after injection into mice. J Parasitol 83:189–193

    CAS  Google Scholar 

  • Tumbar T, Guasch G, Greco V et al (2004) Defining the epithelial stem cell niche in skin. Science 303:359–363

    CAS  Google Scholar 

  • Uhrík B, Rýdlová K, Zacharová D (1989) The roles of haemocytes during degeneration and regeneration of crayfish muscle fibres. Cell Tissue Res 255:443–449

    Google Scholar 

  • Van den Spiegel D, Jangoux M, Flammang P (2000) Maintaining the line of defense: Regeneration of Cuvierian tubules in the sea cucumber Holothuria forskali (Echinodermata, Holothuroidea). Biol Bull 198:34–49

    Google Scholar 

  • Vaughn D, Strathmann RR (2008) Predators induce cloning in echinoderm larvae. Science 319:1503

    CAS  Google Scholar 

  • Vaziri H, Dragowska W, Allsopp RC et al (1994) Evidence for a mitotic clock in human hematopoietic stem cells: Loss of telomeric DNA with age. Proc Natl Acad Sci USA 91:9857–9860

    CAS  Google Scholar 

  • Vickery MS, McClintock JB (1998) Regeneration in metazoan larvae. Nature 394:140

    CAS  Google Scholar 

  • Vickery MS, McClintock JB (2000) Effects of food concentration and availability on the incidence of cloning in planktotrophic larvae of the sea star Pisaster ochraceus. Biol Bull 199:298–304

    CAS  Google Scholar 

  • Vickery MC, Vickery MS, McClintock JB, et al (2001a) Utilization of a novel deuterostome model for the study of regeneration genetics: molecular cloning of genes that are differentially expressed during early stages of larval sea star regeneration Gene 262:73–80

    Google Scholar 

  • Vickery MC, Vickery MS, McClintock JB et al (2001b) Regeneration in echinoderm larvae. Microsc Res Tech 55:464–473

    Google Scholar 

  • Vickery MS, Vickery MCL, McClintock JB (2002) Morphogenesis and organogenesis in the regenerating planktotrophic larvae of asteroids and echinoids. Biol Bull 203:121–133

    Google Scholar 

  • Vogel G (2003) Stem cells. ‘Stemness’ genes still elusive. Science 302:371

    CAS  Google Scholar 

  • Voronina E, Lopez M, Juliano CE et al (2008) Vasa protein expression is restricted to the small micromeres of the sea urchin, but is inducible in other lineages early in development. Dev Biol 314:276–286

    CAS  Google Scholar 

  • Voskoboynik A, Simon-Blecher N, Soen Y et al (2007) Striving for normality: Whole body regeneration through a series of abnormal generations. FASEB J 21:1335–1344

    CAS  Google Scholar 

  • Voskoboynik A, Soen Y, Rinkevich Y et al (2008) Identification of the endostyle as a stem cell niche in a colonial chordate. Cell Stem Cell 3:456–64

    Google Scholar 

  • Wagers AJ, Weissman IL (2004) Plasticity of adult stem cells. Cell 116:639–648

    CAS  Google Scholar 

  • Wang Y, Zayas RM, Guo T et al (2007) Nanos function is essential for development and regeneration of planarian germ cells. Proc Natl Acad Sci USA 104:5901–5906

    CAS  Google Scholar 

  • Weissman IL (2000) Stem cells: Units of development, units of regeneration, and units in evolution. Cell 100:157–168

    CAS  Google Scholar 

  • Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC semantic or structural? Immunol Rev 113:227–241

    CAS  Google Scholar 

  • Wernig M, Meissner A, Foreman R et al (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–324

    CAS  Google Scholar 

  • Wikgren BJP, Gustafsson MKS, Knuts GM (1971) Primary anlage formation in diphyllobothriid tapeworms. Parasitol Res 36:131–139

    Google Scholar 

  • Wittlieb J, Khalturin K, Lohmann JU et al (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci USA 103:6208–6211

    CAS  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 

  • Wray GA, Lowe CJ (2000) Developmental regulatory genes and echinoderm evolution. Syst Biol 49:28–51

    CAS  Google Scholar 

  • Wright RK (1981) Urochordates. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells. Academic Press, London, pp 565–626

    Google Scholar 

  • Wright WE, Piatyszek MA, Rainey WE et al (1996) Telomerase activity in human germline and embryonic tissues and cells. Dev Genet 18:173–179

    CAS  Google Scholar 

  • Young HE, Steele TA, Bray RA et al (1999) Human pluripotent and progenitor cells display cell surface cluster differentiation markers CD10, CD13, CD56, and MHC class-I. Proc Soc Exp Biol Med 221:63–71

    CAS  Google Scholar 

  • Zayas RM, Hernández A, Habermann B et al (2005) The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: Analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 102:18491–18496

    CAS  Google Scholar 

  • Zhang J, Niu C, Ye L et al (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425:836–841

    CAS  Google Scholar 

  • Zhong-Wei D, Hsiao-Chien C, Zhen Y (2001) Identification of putative downstream genes of Oct-4 by suppression-subtractive hybridization. Biochem Biophys Res Commun 282:701–706

    Google Scholar 

  • Zimmermann S, Martens UM (2008) Telomeres, senescence, and hematopoietic stem cells. Cell Tissue Res 331:79–90

    Google Scholar 

  • Zlatanova J, Thakar A (2008) H2A.Z: View from the top. Structure 16:166–179

    CAS  Google Scholar 

Download references

Acknowledgements

Authors acknowledge the support of the Marine Genomics Europe Network of Excellence. VM is gratefull to Rosa Bonaventura for preparation of echinoderm figure pannels and to the MoMa ASI project for partial financial support.

Author information

Authors and Affiliations

  1. Institute for Stem Cells Research and Regenerative Medicine, Stanford University School of Medicine, 94305, Stanford, CA, USA

    Yuval Rinkevich

  2. Consiglio Nazionale delle Ricerche, Istituto di Biomedicina e Immunologia Molecolare “Alberto Monroy”, 90146, Via Ugo La Malfa 153, Palermo, Italy

    Valeria Matranga

  3. Israel Oceanographic & Limnological Research, National Institute of Oceanography, Tel Shikmona, 31080, Haifa, Israel

    Baruch Rinkevich

Authors
  1. Yuval Rinkevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valeria Matranga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baruch Rinkevich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuval Rinkevich .

Editor information

Editors and Affiliations

  1. Limnological Research, Israel Oceanographic & , Haifa, 31 080, Israel

    Baruch Rinkevich

  2. Istituto di Biomedicina e Immunologia, CNR Palermo, Via La Malfa 153, Palermo, 90146, Italy

    Valeria Matranga

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Rinkevich, Y., Matranga, V., Rinkevich, B. (2009). Stem Cells in Aquatic Invertebrates: Common Premises and Emerging Unique Themes. In: Rinkevich, B., Matranga, V. (eds) Stem Cells in Marine Organisms. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2767-2_4

Download citation

Publish with us

Policies and ethics

Search

Navigation