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Post-autotomy regeneration of respiratory trees in the holothurian Apostichopus japonicus (Holothuroidea, Aspidochirotida)

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Abstract

Specialised respiratory organs, viz. the respiratory trees attached to the dorsal part of the cloaca, are present in most holothurians. These organs evolved within the class Holothuroidea and are absent in other echinoderms. Some holothurian species can regenerate their respiratory trees but others lack this ability. Respiratory trees therefore provide a model for investigating the origin and evolution of repair mechanisms in animals. We conducted a detailed morphological study of the regeneration of respiratory trees after their evisceration in the holothurian Apostichopus japonicus. Regeneration of the respiratory trees occurred rapidly and, on the 15th day after evisceration, their length reached 15–20 mm. Repair involved cells of the coelomic and luminal epithelia of the cloaca. Peritoneocytes and myoepithelial cells behaved differently during regeneration: the peritoneocytes kept their intercellular junctions and migrated as a united layer, whereas groups of myoepithelial cells disaggregated and migrated as individual cells. Although myoepithelial cells did not divide during regeneration, the peritoneocytes proliferated actively. The contractile system of the respiratory trees was assumed to develop during regeneration by the migration of myoepithelial cells from the coelomic epithelium of the cloaca. The luminal epithelium of the respiratory trees formed as a result of dedifferentiation, migration and transformation of cells of the cloaca lining. The mode of regeneration of holothurian respiratory trees is discussed.

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References

  • Agata K, Tanaka T, Kobayashi C, Kato K, Saitoh Y (2003) Intercalary regeneration in planarians. Dev Dyn 226:308–316

    Article  PubMed  CAS  Google Scholar 

  • Agata K, Saito Y, Nakajima E (2007) Unifying principles of regeneration. I. Epimorphosis versus morphallaxis. Dev Growth Differ 49:73–78

    PubMed  Google Scholar 

  • Ausich WI (1996) Origin of the class Crinoidea. In: Mooi R, Telford M (eds) Proceedings of 9th International Echinoderm Conference, August 5–9. Califormia Academy of Sciences, San Francisco, p 24

    Google Scholar 

  • Ausich WI, Baumiller TK (1993) Column regeneration in an ordovician crinoid (Echinodermata)—paleobiologic implications. J Paleontol 67:1068–1070

    Google Scholar 

  • Balser EJ (2004) And then there were more: cloning by larvae of echinoderms. In: Heinzeller T, Nebelsick JH (eds) Echinoderms: München. Taylor & Francis, London, pp 3–9

    Google Scholar 

  • Basina YA (1940) A study of regeneration by method of calculation of mitotic coefficient (in Russian). Byull Eksp Biol Med 10:389–391

    Google Scholar 

  • Brockes JP (1998) Progenitor cells for regeneration: origin by reversal of the differentiated state. In: Ferretti P, Géraudie J (eds) Cellular and molecular basis of regeneration: from invertebrates to humans. Wiley, Chichester, pp 63–77

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Candia Carnevali MD (2006) Regeneration in Echinoderms: repair, regrowth, cloning. Invertebrate Survival J 3:64–76

    Google Scholar 

  • Candia Carnevali MD, Bruno L, Donini L, Melone G (1989) Regeneration and morphogenesis in the feather star arm. In: Kiortsis V, Koussoulakos S, Wallace H (eds) Recent trends in regeneration research. Plenum, New York, pp 447–460

    Google Scholar 

  • Carlson BM (1998) Development and regeneration, with special emphasis on the amphibian limb. In: Ferretti P, Géraudie J (eds) Cellular and molecular basis of regeneration: from invertebrates to humans. Wiley, Chichester, pp 45–61

    Google Scholar 

  • Dolmatov IY (1992) Regeneration of the aquapharyngeal complex in the holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirota). In: Taban CH, Boilly B (eds) Keys for regeneration. Monographs in developmental biology, vol 23. Karger, Basel, pp 40–50

    Google Scholar 

  • Dolmatov IY (1995) Ultrastructural organization of contractile systems in the holothurian Eupentacta fraudatrix. Russ J Mar Biol 21:119–123

    Google Scholar 

  • Dolmatov IY (1999) Regeneration in echinoderms. Russ J Mar Biol 25:225–233

    Google Scholar 

  • Dolmatov IY (2009) Regeneration of the digestive system in holothurians. Zh Obshch Biol (in press)

  • Dolmatov IY, Ginanova TT (2001) Regeneration in holothurians. Microsc Res Tech 55:452–463

    Article  PubMed  CAS  Google Scholar 

  • Dolmatov IY, Mashanov VS (2007) Regeneration in holothurians (in Russian). Dalnauka, Vladivostok

    Google Scholar 

  • Dolmatov IY, Eliseikina MG, Bulgakov AA, Ginanova TT, Lamash NE, Korchagin VP (1996) Muscle regeneration in the holothurian Stichopus japonicus. Roux’s Arch Dev Biol 205:486–493

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eliseikina MG, Magarlamov TY, Dolmatov IY (2009) Stem cells of holothuroid coelomocytes. In: Harris LG (ed) Echinoderms: Proceedings from the 12th International Echinoderm Conference, August 2006, Durham, New Hampshire. Routledge, New York (in press)

  • Emson RH, Mladenov PV (1987) Studies of the fissiparous holothurian Holothuria parvula (Selenka) (Echinodermata: Holothuroidea). J Exp Mar Biol Ecol 111:195–211

    Article  Google Scholar 

  • Emson RH, Wilkie IC (1980) Fission and autotomy in echinoderms. Oceanogr Mar Biol Annu Rev 18:155–250

    Google Scholar 

  • Feral JP, Massin C (1982) Digestive system: Holothuroidea. In: Echinoderm nutrition. Balkema, Rotterdam, pp 192–212

    Google Scholar 

  • Frolova LT, Dolmatov IY (2009) The digestive system of the ophiuroid Amphipholis kochii: morphology and regeneration. In: Harris LG (ed) Echinoderms: Proceedings from the 12th International Echinoderm Conference, August 2006, Durham, New Hampshire. Routledge, New York (in press)

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • García-Arrarás JE, Rojas-Soto M, Jiménez LB, Díaz-Miranda L (2001) The enteric nervous system of echinoderms: unexpected complexity revealed by neurochemical analysis. J Exp Biol 204:865–873

    PubMed  Google Scholar 

  • Gibson AW, Burke RD (1983) Gut regeneration by morphallaxis in the sea cucumber Leprosynapta clarki (Heding, 1928). Can J Zool 61:2720–2732

    Article  Google Scholar 

  • Goss RJ (1992) The evolution of regeneration—adaptive or inherent. J Theor Biol 159:241–260

    Article  PubMed  CAS  Google Scholar 

  • Hyman LH (1955) The invertebrates: Echinodermata. The coelome bilateria. McGraw-Hill, New York

    Google Scholar 

  • Kille FR (1935) Regeneration in Thyone briareus (Lesueur) following induced autotomy. Biol Bull 69:82–108

    Article  Google Scholar 

  • Levin VS (1982) Japanese sea cucumber (in Russian). Dalnevostochnoe knizhnoe izdatelstvo, Vladivostok

    Google Scholar 

  • Liozner LD (1982) Regeneration and development (in Russian). Nauka, Moscow

    Google Scholar 

  • Liozner LD, Zamaraev VN (1965) Processes of reorganization during regeneration in planarians (in Russian). Zh Obshch Biol 26:431–436

    Google Scholar 

  • Marushkina NB, Gracheva ND (1978) Autoradiographical study of the proliferative activity of the intestinal epithelium in Stichopus japonicus under normal conditions and after autotomy (in Russian). Tsitologia 20:426–430

    Google Scholar 

  • Mashanov VS, Dolmatov IY, Heinzeller T (2005) Transdifferentiation in holothurian gut regeneration. Biol Bull 209:184–193

    Article  PubMed  Google Scholar 

  • Menton DN, Eisen AZ (1973) Cutaneous wound healing in the sea cucumber Thyone briareus. J Morphol 141:185–204

    Article  PubMed  CAS  Google Scholar 

  • Mladenov PV, Burke RD (1994) Echinodermata: Asexual propagation. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. Oxford & IBH, New Delhi, pp 339–383

    Google Scholar 

  • Morgan TH (1901) Regeneration. Mac-Millan, New York

    Google Scholar 

  • Mozzi D, Dolmatov IY, Bonasoro F, Candia Carnevali MD (2006) Visceral regeneration in the crinoid Antedon mediterranea: basic mechanisms, tissues and cells involved in gut regrowth. Cent Eur J Biol 1:609–635

    Article  Google Scholar 

  • Needham AE (1965) Regeneration in the Arthropoda and its endocrine control. In: Kiortsis V, Trampush HAL (eds) Regeneration in animals and related problems. North-Holland, Amsterdam, pp 283–323

    Google Scholar 

  • Odintsova NA, Dolmatov IY, Mashanov VS (2005) Regenerating holothurian tissues as a source of cells for long-term cell culture. Mar Biol 146:915–921

    Article  Google Scholar 

  • Rieger RM, Lombardi J (1987) Ultrastructure of coelomic lining in echinoderm podia: significance for concepts in the evolution of muscle and peritoneal cells. Zoomorphology 107:191–208

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Smiley S (1994) Holothuroidea. In: Harrison FW, Chia FS (eds) Microscopic anatomy of invertebrates: Echinodermata, vol 14. Wiley-Liss, New York, pp 401–471

    Google Scholar 

  • Spirina IS, Dolmatov IY (2001) Morphology of the respiratory trees in the holothurians Apostichopus japonicus and Cucumaria japonica. Russ J Mar Biol 27:367–375

    Article  Google Scholar 

  • Spirina IS, Dolmatov IY (2003) Mitotic activity in tissues of the regenerating respiratory tree of the holothurian Apostichopus japonicus (Holothuroidea, Aspidochirota). Russ J Mar Biol 29:123–125

    Article  Google Scholar 

  • Shukalyuk AI, Dolmatov IY (2001) Regeneration of the digestive tube in the holothurian Apostichopus japonicus after evisceration. Russ J Mar Biol 27:168–173

    Article  Google Scholar 

  • VandenSpiegel 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 198:31–49

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the anonymous reviewers, whose valuable critical comments enabled us to improve the quality of the manuscript. Our special thanks are extended to Dr. I.C. Wilkie (Glasgow Caledonian University, Scotland) for suggestions and critical reading of the manuscript.

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Correspondence to Igor Y. Dolmatov.

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This work was funded by a grant from the Russian Foundation for Basic Research (project no. 08–04–00284) to I.Y.D. and by a grant from the Far Eastern Branch of the Russian Academy of Sciences and the Russian Foundation for Basic Research (project no. 09–04–98547) to T.T.G.

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Dolmatov, I.Y., Ginanova, T.T. Post-autotomy regeneration of respiratory trees in the holothurian Apostichopus japonicus (Holothuroidea, Aspidochirotida). Cell Tissue Res 336, 41–58 (2009). https://doi.org/10.1007/s00441-009-0761-6

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