Advertisement

Whole-Body Regeneration in the Colonial Tunicate Botrylloides leachii

  • Simon Blanchoud
  • Buki Rinkevich
  • Megan J. Wilson
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)

Abstract

The colonial marine invertebrate Botrylloides leachii belongs to the Tunicata subphylum, the closest invertebrate relatives to the vertebrate group and the only known class of chordates that can undergo whole-body regeneration (WBR). This dramatic developmental process allows a minute isolated fragment of B. leachii’s vascular system, or a colony excised of all adults, to restore a functional animal in as little as 10 days. In addition to this exceptional regenerative capacity, B. leachii can reproduce both sexually, through a tadpole larval stage, and asexually, through palleal budding. Thus, three alternative developmental strategies lead to the establishment of filter-feeding adults. Consequently, B. leachii is particularly well suited for comparative studies on regeneration and should provide novel insights into regenerative processes in chordates.

Here, after a short introduction on regeneration, we overview the biology of B. leachii as well as the current state of knowledge on WBR in this species and in related species of tunicates. Finally, we highlight the possible future directions that research might take in the study of WBR, including thoughts on technological approaches that appear most promising in this context. Overall, we provide a synthesis of the current knowledge on WBR in B. leachii to support research in this chordate species.

Keywords

Whole-body regeneration Botrylloides leachii Chordate Tunicate Ascidian 

Notes

Acknowledgements

We would like to thank Aude Blanchoud for proofreading this review. SB was funded by the Swiss National Science Foundation (SNSF) grant number PZ00P3_17398. MJW was funded by a School of Biomedical Sciences Dean’s bequest grant. BR was funded by the Israel Academy of Sciences grant number 172/17. SB, MJW and BR were funded by a Royal Society of NZ Marsden fund grant (UOO1713).

References

  1. Bely AE, Nyberg KG (2010) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25:161–170.  https://doi.org/10.1016/j.tree.2009.08.005CrossRefPubMedGoogle Scholar
  2. Berna L, Alvarez-Valin F (2014) Evolutionary genomics of fast evolving tunicates. Genome Biol Evol 6:1724–1738.  https://doi.org/10.1093/gbe/evu122CrossRefPubMedPubMedCentralGoogle Scholar
  3. Berrill NJ (1947) The developmental cycle of Botrylloides. Q J Microsc Sci 88:393–407PubMedGoogle Scholar
  4. Berrill NJ, Cohen A (1936) Regeneration in Clavelina lepadiformis. J Exp Biol 13:352–362Google Scholar
  5. Blanchoud S, Zondag L, Lamare MD, Wilson MJ (2017) Hematological analysis of the ascidian Botrylloides leachii (Savigny, 1816) during whole-body regeneration. Biol Bull 232:143–157.  https://doi.org/10.1086/692841CrossRefPubMedGoogle Scholar
  6. Brewin BI (1946) Ascidians in the vicinity of the Portobello Marine Biological Station, Otago Harbour. Trans R Soc N Z 76:87–131Google Scholar
  7. Brockes JP, Kumar A, Velloso CP (2001) Regeneration as an evolutionary variable. J Anat 199:3–11.  https://doi.org/10.1017/S0021878201008299CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brown FD, Swalla BJ (2012) Evolution and development of budding by stem cells: ascidian coloniality as a case study. Dev Biol 369:151–162.  https://doi.org/10.1016/j.ydbio.2012.05.038CrossRefPubMedGoogle Scholar
  9. Brown FD, Keeling EL, Le AD, Swalla BJ (2009) Whole body regeneration in a colonial ascidian, Botrylloides violaceus. J Exp Zool B Mol Dev Evol 312:885–900.  https://doi.org/10.1002/jez.b.21303CrossRefPubMedGoogle Scholar
  10. Brunetti R (1976) Biological cycle of Botrylloides leachi (Savigny) (Ascidiacea) in the Venetian lagoon. Vie Milieu XXVI:105–122Google Scholar
  11. Burighel P, Brunetti R, Zaniolo G (1976) Hibernation of the colonial ascidian Botrylloides leachi (Savigny): histological observations. Ital J Zool 43:293–301.  https://doi.org/10.1080/11250007609430146CrossRefGoogle Scholar
  12. Chambon J-P, Nakayama A, Takamura K et al (2007) ERK- and JNK-signalling regulate gene networks that stimulate metamorphosis and apoptosis in tail tissues of ascidian tadpoles. Development 134:1203–1219.  https://doi.org/10.1242/dev.002220CrossRefPubMedGoogle Scholar
  13. Cima F, Perin A, Burighel P, Ballarin L (2002) Morpho-functional characterization of haemocytes of the compound ascidian Botrylloides leachi (Tunicata, Ascidiacea). Acta Zool 82:261–274.  https://doi.org/10.1046/j.1463-6395.2001.00087.xCrossRefGoogle Scholar
  14. Davidson B, Swalla BJ (2002) A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Development 129:4739–4751CrossRefGoogle Scholar
  15. Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968.  https://doi.org/10.1038/nature04336CrossRefPubMedGoogle Scholar
  16. Franchi N, Ballin F, Manni L et al (2016) Recurrent phagocytosis-induced apoptosis in the cyclical generation change of the compound ascidian Botryllus schlosseri. Dev Comp Immunol 62:8–16.  https://doi.org/10.1016/j.dci.2016.04.011CrossRefPubMedGoogle Scholar
  17. Franchi N, Ballin F, Ballarin L (2017) Protection from oxidative stress in immunocytes of the colonial ascidian Botryllus schlosseri: transcript characterization and expression studies. Biol Bull 232:45–57.  https://doi.org/10.1086/691694CrossRefPubMedGoogle Scholar
  18. Freeman G (1964) The role of blood cells in the process of asexual reproduction in the tunicate Perophora viridis. J Exp Zool 156:157–183.  https://doi.org/10.1002/jez.1401560204CrossRefPubMedGoogle Scholar
  19. Galliot B (2013) Regeneration in hydra. In: eLS. Wiley, ChichesterGoogle Scholar
  20. Gasparini F, Burighel P, Manni L, Zaniolo G (2008) Vascular regeneration and angiogenic-like sprouting mechanism in a compound ascidian is similar to vertebrates. Evol Dev 10:591–605.  https://doi.org/10.1111/j.1525-142X.2008.00274.xCrossRefPubMedGoogle Scholar
  21. Gasparini F, Caicci F, Rigon F et al (2014) Testing an unusual in vivo vessel network model: a method to study angiogenesis in the colonial tunicate Botryllus schlosseri. Sci Rep 4:6460.  https://doi.org/10.1038/srep06460CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gutierrez S, Brown FD (2017) Vascular budding in Symplegma brakenhielmi and the evolution of coloniality in styelid ascidians. Dev Biol 423:152–169.  https://doi.org/10.1016/j.ydbio.2017.01.012CrossRefPubMedGoogle Scholar
  23. Jaźwińska A, Sallin P (2016) Regeneration versus scarring in vertebrate appendages and heart. J Pathol 238:233–246.  https://doi.org/10.1002/path.4644CrossRefPubMedGoogle Scholar
  24. Kassmer SH, Rodriguez D, De Tomaso AW (2016) Colonial ascidians as model organisms for the study of germ cells, fertility, whole body regeneration, vascular biology and aging. Curr Opin Genet Dev 39:101–106.  https://doi.org/10.1016/j.gde.2016.06.001CrossRefPubMedGoogle Scholar
  25. Kawamura K, Fujiwara S (1994) Transdifferentiation of pigmented multipotent epithelium during morphallactic development of budding tunicates. Int J Dev Biol 38:369–377PubMedGoogle Scholar
  26. Kawamura K, Fujiwara S (1995) Cellular and molecular characterization of transdifferentiation in the process of morphallaxis of budding tunicates. Semin Cell Dev Biol 6:117–126.  https://doi.org/10.1006/scel.1995.0017CrossRefGoogle Scholar
  27. Kawamura K, Hayata D, Fujiwara S, Yubisui T (1998) Serine protease inhibitors expressed in the process of budding of tunicates as revealed by EST analysis. J Biochem 124:1004–1012.  https://doi.org/10.1093/oxfordjournals.jbchem.a022192CrossRefPubMedGoogle Scholar
  28. Kawamura K, Kariya Y, Ono Y et al (2006) Molecular collaborations between serpins and trefoil factor promote endodermal cell growth and gastrointestinal differentiation in budding tunicates. Develop Growth Differ 48:309–322.  https://doi.org/10.1111/j.1440-169X.2006.00865.xCrossRefGoogle Scholar
  29. Kawamura K, Sugino Y, Sunanaga T, Fujiwara S (2008) Multipotent epithelial cells in the process of regeneration and asexual reproduction in colonial tunicates. Develop Growth Differ 50:1–11.  https://doi.org/10.1111/j.1440-169X.2007.00972.xCrossRefGoogle Scholar
  30. Kawamura K, Tiozzo S, Manni L et al (2011) Germline cell formation and gonad regeneration in solitary and colonial ascidians. Dev Dyn 240:299–308.  https://doi.org/10.1002/dvdy.22542CrossRefPubMedGoogle Scholar
  31. Kawamura K, Yoshida T, Sekida S (2018) Autophagic dedifferentiation induced by cooperation between TOR inhibitor and retinoic acid signals in budding tunicates. Dev Biol 433:384–393.  https://doi.org/10.1016/j.ydbio.2017.08.023CrossRefPubMedGoogle Scholar
  32. Kürn U, Rendulic S, Tiozzo S, Lauzon RJ (2011) Asexual propagation and regeneration in colonial ascidians. Biol Bull 221:43–61.  https://doi.org/10.1086/BBLv221n1p43CrossRefPubMedGoogle Scholar
  33. Laird DJ, Weissman IL (2004) Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate Botryllus schlosseri. Dev Biol 273:185–194.  https://doi.org/10.1016/j.ydbio.2004.05.029CrossRefPubMedGoogle Scholar
  34. Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a colonial ascidian. Cell 123:1351–1360.  https://doi.org/10.1016/j.cell.2005.10.026CrossRefPubMedGoogle Scholar
  35. Lauzon RJ, Ishizuka KJ, Weissman IL (2002) Cyclical generation and degeneration of organs in a colonial urochordate involves crosstalk between old and new: a model for development and regeneration. Dev Biol 249:333–348.  https://doi.org/10.1006/dbio.2002.0772CrossRefPubMedGoogle Scholar
  36. Lauzon RJ, Brown C, Kerr L, Tiozzo S (2013) Phagocyte dynamics in a highly regenerative urochordate: insights into development and host defense. Dev Biol 374:357–373.  https://doi.org/10.1016/j.ydbio.2012.11.006CrossRefPubMedGoogle Scholar
  37. 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.  https://doi.org/10.1002/dvdy.21037CrossRefPubMedGoogle Scholar
  38. Michaelsen W, Stephenson TA (1934) The ascidians of the Cape Province of South Africa. Trans R Soc South Afr 22:129–163.  https://doi.org/10.1080/00359193409519335CrossRefGoogle Scholar
  39. Milkman R (1967) Genetic and developmental studies on Botryllus schlosseri. Biol Bull 132:229.  https://doi.org/10.2307/1539891CrossRefPubMedGoogle Scholar
  40. Millar RH (1971) The biology of ascidians. Adv Mar Biol 9:1–100.  https://doi.org/10.1016/S0065-2881(08)60341-7CrossRefGoogle Scholar
  41. Mukai H (1977) Comparative studies on the structure of reproductive organs of four botryllid ascidians. J Morphol 152:363–379.  https://doi.org/10.1002/jmor.1051520307CrossRefPubMedGoogle Scholar
  42. Mukai H, Sugimoto K, Taneda Y (1978) Comparative studies on the circulatory system of the compound ascidians, Botryllus, Botrylloides and Symplegma. J Morphol 157:49–78.  https://doi.org/10.1002/jmor.1051570105CrossRefGoogle Scholar
  43. Mukai H, Saito Y, Watanabe H (1987) Viviparous development in Botrylloides (compound ascidians). J Morphol 193:263–276.  https://doi.org/10.1002/jmor.1051930305CrossRefPubMedGoogle Scholar
  44. Murphy K (2012) Innate immunity: the first lines of defense. In: Janeway’s immunobiology. Taylor & Francis, Oxford, pp 37–73Google Scholar
  45. Myers PE (1990) Space versus other limiting resources for a colonial tunicate, Botrylloides leachii (Savigny), on fouling plates. J Exp Mar Bio Ecol 141:47–52.  https://doi.org/10.1016/0022-0981(90)90156-7CrossRefGoogle Scholar
  46. Nakayama A, Satou Y, Satoh N (2002) Further characterization of genes expressed during Ciona intestinalis metamorphosis. Differentiation 70:429–437.  https://doi.org/10.1046/j.1432-0436.2002.700805.xCrossRefPubMedGoogle Scholar
  47. Ohashi M, Kawamura K, Fujii N et al (1999) A retinoic acid-inducible modular protease in budding ascidians. Dev Biol 214:38–45.  https://doi.org/10.1006/dbio.1999.9400CrossRefPubMedGoogle Scholar
  48. Oka H, Watanabe H (1957) Vascular budding, a new type of budding in Botryllus. Biol Bull 112:225–240.  https://doi.org/10.2307/1539200CrossRefGoogle Scholar
  49. Oka H, Watanabe H (1959) Vascular budding in Botrylloides. Biol Bull 117:340.  https://doi.org/10.2307/1538913CrossRefGoogle Scholar
  50. Okuyama M, Saito Y (2001) Studies on Japanese botryllid ascidians. I. A new species of the genus Botryllus from the Izu Islands. Zool Sci 18:261–267.  https://doi.org/10.2108/zsj.18.261CrossRefGoogle Scholar
  51. Oren M, Douek J, Fishelson Z, Rinkevich B (2007) Identification of immune-relevant genes in histoincompatible rejecting colonies of the tunicate Botryllus schlosseri. Dev Comp Immunol 31:889–902.  https://doi.org/10.1016/j.dci.2006.12.009CrossRefPubMedGoogle Scholar
  52. Paz G, Rinkevich B (2002) Morphological consequences for multi-partner chimerism in Botrylloides, a colonial urochordate. Dev Comp Immunol 26:615–622CrossRefGoogle Scholar
  53. Poss KD (2010) Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat Rev Genet 11:710–722.  https://doi.org/10.1038/nrg2879CrossRefPubMedPubMedCentralGoogle Scholar
  54. Rabinowitz C, Rinkevich B (2003) Epithelial cell cultures from Botryllus schlosseri palleal buds: accomplishments and challenges. Methods Cell Sci 25:137–148.  https://doi.org/10.1007/s11022-004-2087-9CrossRefPubMedGoogle Scholar
  55. Rabinowitz C, Rinkevich B (2004) In vitro delayed senescence of extirpated buds from zooids of the colonial tunicate Botryllus schlosseri. J Exp Biol 207:1523–1532.  https://doi.org/10.1242/jeb.00899CrossRefPubMedGoogle Scholar
  56. Rabinowitz C, Rinkevich B (2011) De novo emerged stemness signatures in epithelial monolayers developed from extirpated palleal buds. In Vitro Cell Dev Biol Anim 47:26–31.  https://doi.org/10.1007/s11626-010-9357-4CrossRefPubMedGoogle Scholar
  57. Rabinowitz C, Alfassi G, Rinkevich B (2009) Further portrayal of epithelial monolayers emergent de novo from extirpated ascidians palleal buds. In Vitro Cell Dev Biol Anim 45:334–342.  https://doi.org/10.1007/s11626-009-9179-4CrossRefPubMedGoogle Scholar
  58. Rinkevich B, Rinkevich Y (2013) The “Stars and Stripes” metaphor for animal regeneration-Elucidating two fundamental strategies along a continuum. Cells 2:1–18.  https://doi.org/10.3390/cells2010001CrossRefGoogle Scholar
  59. Rinkevich B, Shapira M (1998) An improved diet for inland broodstock and the establishment of an inbred line from a colonial sea squirt (Ascidiacea). Aquat Living Resour 11:163–171.  https://doi.org/10.1016/S0990-7440(98)80113-7CrossRefGoogle Scholar
  60. Rinkevich B, Weissman IL (1987) A long-term study on fused subclones in the ascidian Botryllus schlosseri: the resorption phenomenon (Protochordata: Tunicata). J Zool 213:717–733.  https://doi.org/10.1111/j.1469-7998.1987.tb03736.xCrossRefGoogle Scholar
  61. Rinkevich B, Shlemberg Z, Lilkerlevav T et al (1993) Life-history characteristics of Botrylloides (Tunicata) populations in Akko Bay, Mediterranean coast of Israel. Isr J Zool 39:197–212.  https://doi.org/10.1080/00212210.1993.10688712CrossRefGoogle Scholar
  62. Rinkevich B, Shlemberg Z, Fishelson L (1995) Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci USA 92:7695–7699CrossRefGoogle Scholar
  63. Rinkevich Y, Douek J, Haber O et al (2007a) Urochordate whole body regeneration inaugurates a diverse innate immune signaling profile. Dev Biol 312:131–146.  https://doi.org/10.1016/j.ydbio.2007.09.005CrossRefPubMedGoogle Scholar
  64. Rinkevich Y, Paz G, Rinkevich B, Reshef R (2007b) Systemic bud induction and retinoic acid signaling underlie whole body regeneration in the urochordate Botrylloides leachi. PLoS Biol 5:e71.  https://doi.org/10.1371/journal.pbio.0050071CrossRefPubMedPubMedCentralGoogle Scholar
  65. Rinkevich Y, Rinkevich B, Reshef R (2008) Cell signaling and transcription factor genes expressed during whole body regeneration in a colonial chordate. BMC Dev Biol 8:100.  https://doi.org/10.1186/1471-213X-8-100CrossRefPubMedPubMedCentralGoogle Scholar
  66. Rinkevich Y, Rosner A, Rabinowitz C et al (2010) Piwi positive cells that line the vasculature epithelium, underlie whole body regeneration in a basal chordate. Dev Biol 345:94–104.  https://doi.org/10.1016/j.ydbio.2010.05.500CrossRefPubMedGoogle Scholar
  67. Rinkevich Y, Voskoboynik A, Rosner A et al (2013) Repeated, long-term cycling of putative stem cells between niches in a basal chordate. Dev Cell 24:76–88.  https://doi.org/10.1016/j.devcel.2012.11.010CrossRefPubMedGoogle Scholar
  68. Roberts B, Davidson B, MacMaster G et al (2007) A complement response may activate metamorphosis in the ascidian Boltenia villosa. Dev Genes Evol 217:449–458.  https://doi.org/10.1007/s00427-007-0157-0CrossRefPubMedGoogle Scholar
  69. Rosner A, Rinkevich B (2007) The DDX3 subfamily of the DEAD box helicases: divergent roles as unveiled by studying different organisms and in vitro assays. Curr Med Chem 14:2517–2525.  https://doi.org/10.2174/092986707782023677CrossRefPubMedGoogle Scholar
  70. Rosner A, Rinkevich B (2011) VASA as a specific marker for germ cells lineage: in light of evolution. Trends Comp Biochem Physiol 15:1–15Google Scholar
  71. Rosner A, Paz G, Rinkevich B (2006) Divergent roles of the DEAD-box protein BS-PL10, the urochordate homologue of human DDX3 and DDX3Y proteins, in colony astogeny and ontogeny. Dev Dyn 235:1508–1521.  https://doi.org/10.1002/dvdy.20728CrossRefPubMedGoogle Scholar
  72. Rosner A, Moiseeva E, Rinkevich Y et al (2009) Vasa and the germ line lineage in a colonial urochordate. Dev Biol 331:113–128.  https://doi.org/10.1016/j.ydbio.2009.04.025CrossRefPubMedGoogle Scholar
  73. Rosner A, Moiseeva E, Rabinowitz C, Rinkevich B (2013) Germ lineage properties in the urochordate Botryllus schlosseri - from markers to temporal niches. Dev Biol 384:356–374.  https://doi.org/10.1016/j.ydbio.2013.10.002CrossRefPubMedGoogle Scholar
  74. Rosner A, Alfassi G, Moiseeva E et al (2014) The involvement of three signal transduction pathways in botryllid ascidian astogeny, as revealed by expression patterns of representative genes. Int J Dev Biol 58:669–676.  https://doi.org/10.1387/ijdb.140114arCrossRefGoogle Scholar
  75. Roy S, Gatien S (2008) Regeneration in axolotls: a model to aim for! Exp Gerontol 43:968–973.  https://doi.org/10.1016/j.exger.2008.09.003CrossRefPubMedGoogle Scholar
  76. Rychel AL, Swalla BJ (2009) Regeneration in hemichordates and echinoderms. In: Stem cells in marine organisms. Springer Netherlands, Dordrecht, pp 245–265CrossRefGoogle Scholar
  77. Saito Y, Watanabe H (1985) Studies on Japanese compound styelid ascidians. IV. Three new species of the genus Botrylloides from the vicinity of Shimoda. Publ Seto Mar Biol Lab 30:227–240CrossRefGoogle Scholar
  78. Saito Y, Hirose E, Watanabe H (1994) Allorecognition in compound ascidians. Int J Dev Biol 38:237–247PubMedGoogle Scholar
  79. Sánchez Alvarado A (2000) Regeneration in the metazoans: why does it happen? Bioessays 22:578–590CrossRefGoogle Scholar
  80. Sánchez Alvarado A, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7:873–884.  https://doi.org/10.1038/nrg1923CrossRefPubMedGoogle Scholar
  81. Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295.  https://doi.org/10.1038/nrg1042CrossRefPubMedGoogle Scholar
  82. Satoh N (2011) Tunicate embryos and cell specification. In: eLS. Wiley, ChichesterGoogle Scholar
  83. Savigny J-C (1816) Mémoires sur les animaux sans vertèbres. G. Dufour, ParisGoogle Scholar
  84. Sawada H, Yokosawa H, Lambert CC (2001) The biology of ascidians. Springer, TokyoCrossRefGoogle Scholar
  85. Seifert AW, Kiama SG, Seifert MG et al (2012) Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489:561–565.  https://doi.org/10.1038/nature11499CrossRefPubMedPubMedCentralGoogle Scholar
  86. Slack JM (2017) Animal regeneration: ancestral character or evolutionary novelty? EMBO Rep 18:e201643795.  https://doi.org/10.15252/embr.201643795CrossRefGoogle Scholar
  87. Stolfi A, Gandhi S, Salek F, Christiaen L (2014) Tissue-specific genome editing in Ciona embryos by CRISPR/Cas9. Development 141:4115–4120.  https://doi.org/10.1242/dev.114488CrossRefPubMedPubMedCentralGoogle Scholar
  88. 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.  https://doi.org/10.1073/pnas.96.16.9148CrossRefPubMedGoogle Scholar
  89. 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. Develop Growth Differ 52:603–614.  https://doi.org/10.1111/j.1440-169X.2010.01196.xCrossRefGoogle Scholar
  90. Tamilselvi M, Sivakumar V (2011) Distribution of alien tunicates (Ascidians) in Tuticorin coast, India. World J Zool 6:164–172Google Scholar
  91. Tiozzo S, Brown FD, De Tomaso AW (2008a) Regeneration and stem cells in ascidians. In: Stem Cells. Springer Netherlands, Dordrecht, pp 95–112CrossRefGoogle Scholar
  92. Tiozzo S, Voskoboynik A, Brown FD, De Tomaso AW (2008b) A conserved role of the VEGF pathway in angiogenesis of an ectodermally-derived vasculature. Dev Biol 315:243–255.  https://doi.org/10.1016/j.ydbio.2007.12.035CrossRefPubMedPubMedCentralGoogle Scholar
  93. Tsonis PA (2000) Regeneration in vertebrates. Dev Biol 221:273–284.  https://doi.org/10.1006/dbio.2000.9667CrossRefPubMedGoogle Scholar
  94. Voskoboynik A, Weissman IL (2015) Botryllus schlosseri, an emerging model for the study of aging, stem cells, and mechanisms of regeneration. Invertebr Reprod Dev 59:33–38.  https://doi.org/10.1080/07924259.2014.944673CrossRefPubMedGoogle Scholar
  95. Voskoboynik A, Rinkevich B, Weiss A et al (2004) Macrophage involvement for successful degeneration of apoptotic organs in the colonial urochordate Botryllus schlosseri. J Exp Biol 207:2409–2416.  https://doi.org/10.1242/jeb.01045CrossRefPubMedGoogle Scholar
  96. 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.  https://doi.org/10.1096/fj.06-7337comCrossRefPubMedGoogle Scholar
  97. 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 3:456–464.  https://doi.org/10.1016/j.stem.2008.07.023CrossRefPubMedPubMedCentralGoogle Scholar
  98. Zaniolo G, Manni L, Burighel P (1994) Ovulation and embryo-parent relationships in Botrylloides leachi (Ascidiacea, Tunicata). Invertebr Reprod Dev 25:215–225.  https://doi.org/10.1080/07924259.1994.9672388CrossRefGoogle Scholar
  99. Zondag LE, Rutherford K, Gemmell NJ, Wilson MJ (2016) Uncovering the pathways underlying whole body regeneration in a chordate model, Botrylloides leachi using de novo transcriptome analysis. BMC Genomics 17:114.  https://doi.org/10.1186/s12864-016-2435-6CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Simon Blanchoud
    • 1
  • Buki Rinkevich
    • 2
  • Megan J. Wilson
    • 3
  1. 1.Department of BiologyUniversity of FribourgFribourgSwitzerland
  2. 2.Israel Oceanographic and Limnological ResearchNational Institute of OceanographyHaifaIsrael
  3. 3.Department of Anatomy, School of Biomedical SciencesUniversity of OtagoDunedinNew Zealand

Personalised recommendations