Abstract
Echinoderms are well known as being able to regenerate body parts and thus provide excellent models for studying regenerative processes in adult organisms. We are interested in intestinal regeneration in the sea cucumber, Holothuria glaberrima, and focus here on the regeneration of intestinal muscle components. We have used immunohistochemical techniques to describe the formation of the intestinal muscle layers. Myoblasts are first observed within the regenerating structure, adjacent to the coelomic epithelia. Within a few days, these cells acquire muscle markers and form a single cell layer that underlies the epithelia. Animals injected with BrdU at various regeneration stages have been subsequently analyzed for the presence of muscle differentiation markers. BrdU-labeled muscle nuclei are observed in myocytes of 3-week regenerates, showing that these cells originate from proliferating precursors. The peak in muscle precursor proliferation appears to occur during the second week of regeneration. Therefore, new muscle cells in the regenerating intestine originate from precursors that have undergone cell division. Our results suggest that the precursor cells arise from the coelomic epithelia. We also provide a comparative view of muscle regeneration in an echinoderm, a topic of interest in view of the many recent studies of muscle regeneration in vertebrate species.
Similar content being viewed by others
References
Brockes JP, Kumar A (2002) Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat Rev 3:566–574
Candia-Carnevali MD, Bonasoro F (2001) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426
Candia-Carnevali MD, Lucca E, Bonasoro F (1993) Mechanism of arm regeneration in the feather star Antendon mediterranea: healing of wound and early stages of development. J Exp Zool 267:299–317
Candia-Carnevali MD, Bonasoro F, Lucca E, Thorndyke MC (1995) Pattern of cell proliferation in the early stages of arm regeneration in the feather star Antendon mediterranea. J Exp Zool 272:464–474
Candia-Carnevali MD, Bonasoro F, Biale A (1997) Pattern of bromodeoxyuridine incorporation in the advanced stages of arm regeneration in the feather star Antendon mediterranea. Cell Tissue Res 289:363–374
Candia-Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC (1998) Cellular and molecular mechanisms of arm regeneration in crinoid echinoderms: the potential of arm explants. Dev Genes Evol 208:421–430
Carlson BM (2003) Muscle regeneration in amphibians and mammals: passing the torch. Dev Dyn 226:167–181
Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238
Corbel SY, Lee A, Yi L, Duenas J, Brazelton TR, Blau HM Rossi FM (2003) Contribution of hematopoietic stem cells to skeletal muscle. Nat Med 9:1528–1532
Dolmatov Y (1992) Regeneration of aquapharyngeal complex in the holothurian Eupentacta fraudatrix (Holothuria, Dendrochirota). Monogr Dev Biol 23:40–50
Dolmatov IY, Ginanova TT (2001) Muscle regeneration in holothurians. Microsc Res Tech 55:452–463
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
García-Arrarás JE (1993) Localization of peptides: double labeling immunohistochemistry. In: De Pablo F, Scanes C, Weintraub B (eds) Handbook of endocrine research techniques. Academic Press, San Diego, pp 207–225
García-Arrarás JE, Greenberg MJ (2001) Visceral regeneration in holothurians. Microsc Res Tech 55:438–451
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
García-Arrarás JE, Díaz-Miranda L, Torres-Vázquez I, File S, Jiménez L, Rivera-Bermudez K, Arroyo E, Cruz W (1999) Regeneration of the enteric nervous system in the sea cucumber Holothuria glaberrima. J Comp Neurol 406:461–475
Gojo S, Umezawa A (2003) Plasticity of mesenchymal stem cells: regenerative medicine for diseased hearts. Hum Cell 16:23–30
Ground MD, White JD, Rosenthal N, Bogoyevitch MA (2002) The role of stem cells in skeletal and cardiac muscle repair. J Histochem Cytochem 50:589–610
Hyman L (1955) The invertebrates: echinodermata. McGraw-Hill, New York
Kordylewski L (1983) Light and electron microscopic observations of the development of intestinal musculature in Xenopus. Z Mikrosk Anat Forsch 97:719–734
Kumar A, Velloso CP, Imokawa Y, Brockes JP (2000) Plasticity of retrovirus-labelled myotubes in the newt limb regeneration blastema. Dev Biol 218:125–136
LaBarge MA, Blau HM (2002) Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111:589–601
Leibson NL (1992) Regeneration of digestive tube in holothurians Stichopus japonicus and Eupentacta fraudatrix. In: Taban CH, Boilly B (eds) Keys for regeneration. Monographs in developmental biology, vol 23. Basel, Karger, pp 51–61
Mashanov VS, Dolmatov IY (2001) Regeneration of digestive tract in the pentactulae of the Far-Eastern holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirota). Invertebrate Reprod Dev 39:143–151
Mladenov PV, Bisgrove B, Asotra S, Burke R (1989) Mechanisms of the arm-tip regeneration in the sea star, Leptasterias hexactis. Rouxs Arch Dev Biol 198:19–28
Moss C, Hunter AJ, Thorndyke MC (1998) Patterns of bromodeoxyuridine incorporation and neuropeptide immunoreactivity during arm regeneration in the starfish Asterias rubens. Philos Trans R Soc Lond Biol 353:421–436
Quiñones JL, Rosa R, Ruíz DC, García-Arrarás JE (2002) Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol 250:181–197
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
Sanchez-Alvarado A (2000) Regeneration in the metazoans: why does it happen? Bioessays 22:578–590
Smiley S (1994) Holothuroidea. In: Harrison FW, Chia F-S (eds) Microscopic anatomy of invertebrates, vol 14. Wiley-Liss, New York, pp 401–471
Tsonis PA (2000) Regeneration in vertebrates. Dev Biol 221:273–284
Uhrik B, Rydlova K, Zacharova D (1989) The roles of haemocytes during degeneration and regeneration of crayfish muscle fibers. Cell Tissue Res 255:443–449
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 198:34–49
Acknowledgments
We thank Irma Torres and Griselle Valentín for technical support in the preparation of antibodies and tissue sections, and José Serrano, Andres Batista, and Luis R. Rodríguez for the preparation of figures.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by NSF (IBN-0110692) and NIH-MBRS (S06GM08102). We also acknowledge partial support from NIH-RCMI (RRO-3641-01) and the University of Puerto Rico
Rights and permissions
About this article
Cite this article
Murray, G., García-Arrarás, J.E. Myogenesis during holothurian intestinal regeneration. Cell Tissue Res 318, 515–524 (2004). https://doi.org/10.1007/s00441-004-0978-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-004-0978-3