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Holothurians as a Model System to Study Regeneration

  • José E. García-Arrarás
  • María I. Lázaro-Peña
  • Carlos A. Díaz-Balzac
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)

Abstract

Echinoderms possess an incredible regenerative capacity. Within this phylum, holothurians, better known as sea cucumbers, can regenerate most of their internal and external organs. While regeneration has been studied in several species, the most recent and extensive studies have been done in the species Holothuria glaberrima, the focus of most of our discussion. This chapter presents the model system and integrates the work that has been done to determine the major steps that take place, during regeneration of the intestinal and nervous system, from wound healing to the reestablishment of original function. We describe the cellular and molecular events associated with the regeneration processes and also describe the techniques that have been used, discuss the results, and explain the gaps in our knowledge that remain. We expect that the information provided here paves the road for new and young investigators to continue the study of the amazing potential of regeneration in members of the Echinodermata and how these studies will shed some light into the mechanisms that are common to many regenerative processes.

References

  1. Bai MM (1971) Regeneration in the holothurian, Holothuria scabra Jager. Indian J Exp Biol 9(4):467–471PubMedGoogle Scholar
  2. Bello SA, Abreu-Irizarry RJ, Garcia-Arraras JE (2015) Primary cell cultures of regenerating holothurian tissues. Methods Mol Biol 1189:283–297.  https://doi.org/10.1007/978-1-4939-1164-6_19CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bertolini F (1930) Rigenerazione dell’apparato digerente nello Stichopus regalis. Pubb Staz Zool Napoli 10:439–448Google Scholar
  4. Bertolini F (1932) Rigenerazione dell’apparato digerente nelle Holothuria. Pubb Staz Zool Napoli 11:432–444Google Scholar
  5. Cabrera-Serrano A, Garcia-Arraras JE (2004) RGD-containing peptides inhibit intestinal regeneration in the sea cucumber Holothuria glaberrima. Dev Dyn 231(1):171–178.  https://doi.org/10.1002/dvdy.20112CrossRefPubMedGoogle Scholar
  6. Candelaria AG, Murray G, File SK, Garcia-Arraras JE (2006) Contribution of mesenterial muscle dedifferentiation to intestine regeneration in the sea cucumber Holothuria glaberrima. Cell Tissue Res 325(1):55–65.  https://doi.org/10.1007/s00441-006-0170-zCrossRefPubMedGoogle Scholar
  7. Cannon JT, Kocot KM, Waits DS, Weese DA, Swalla BJ, Santos SR, Halanych KM (2014) Phylogenomic resolution of the hemichordate and echinoderm clade. Curr Biol 24(23):2827–2832.  https://doi.org/10.1016/j.cub.2014.10.016CrossRefPubMedGoogle Scholar
  8. Dawbin WH (1949) Auto-evisceration and the regeneration of viscera in the holothurian Stichopus mollis (Hutton). Trans R Soc N Z 77(4):497–523Google Scholar
  9. Diaz-Balzac CA, Santacana-Laffitte G, San Miguel-Ruiz JE, Tossas K, Valentin-Tirado G, Rives-Sanchez M, Mesleh A, Torres II, Garcia-Arraras JE (2007) Identification of nerve plexi in connective tissues of the sea cucumber Holothuria glaberrima by using a novel nerve-specific antibody. Biol Bull 213(1):28–42.  https://doi.org/10.2307/25066616CrossRefPubMedGoogle Scholar
  10. Diaz-Balzac CA, Abreu-Arbelo JE, Garcia-Arraras JE (2010a) Neuroanatomy of the tube feet and tentacles in Holothuria glaberrima (Holothuroidea, Echinodermata). Zoomorphology 129(1):33–43.  https://doi.org/10.1007/s00435-009-0098-4CrossRefPubMedPubMedCentralGoogle Scholar
  11. Diaz-Balzac CA, Mejias W, Jimenez LB, Garcia-Arraras JE (2010b) The catecholaminergic nerve plexus of Holothuroidea. Zoomorphology 129(2):99–109.  https://doi.org/10.1007/s00435-010-0103-yCrossRefPubMedPubMedCentralGoogle Scholar
  12. Diaz-Balzac CA, Lazaro-Pena MI, Garcia-Rivera EM, Gonzalez CI, Garcia-Arraras JE (2012) Calbindin-D32k is localized to a subpopulation of neurons in the nervous system of the sea cucumber Holothuria glaberrima (Echinodermata). PLoS One 7(3):e32689.  https://doi.org/10.1371/journal.pone.0032689CrossRefPubMedPubMedCentralGoogle Scholar
  13. Diaz-Balzac CA, Vazquez-Figueroa LD, Garcia-Arraras JE (2014) Novel markers identify nervous system components of the holothurian nervous system. Invert Neurosci 14(2):113–125.  https://doi.org/10.1007/s10158-014-0169-1CrossRefPubMedPubMedCentralGoogle Scholar
  14. Diaz-Balzac CA, Lazaro-Pena MI, Vazquez-Figueroa LD, Diaz-Balzac RJ, Garcia-Arraras JE (2016) Holothurian Nervous System Diversity Revealed by Neuroanatomical Analysis. PLoS One 11(3):e0151129.  https://doi.org/10.1371/journal.pone.0151129CrossRefPubMedPubMedCentralGoogle Scholar
  15. Diaz-Miranda L, Garcia-Arraras JE (1995) Pharmacological action of the heptapeptide GFSKLYFamide in the muscle of the sea cucumber Holothuria glaberrima (Echinodermata). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 110(2):171–176CrossRefGoogle Scholar
  16. Diaz-Miranda L, Price DA, Greenberg MJ, Lee TD, Doble KE, Garcia-Arraras JE (1992) Characterization of two novel neuropeptides from the sea cucumber Holothuria glaberrima. Biol Bull 182(2):241–247.  https://doi.org/10.2307/1542117CrossRefPubMedGoogle Scholar
  17. Diaz-Miranda L, Blanco RE, Garcia-Arraras JE (1995) Localization of the heptapeptide GFSKLYFamide in the sea cucumber Holothuria glaberrima (Echinodermata): a light and electron microscopic study. J Comp Neurol 352(4):626–640.  https://doi.org/10.1002/cne.903520410CrossRefPubMedGoogle Scholar
  18. Diaz-Miranda L, Pardo-Reoyo CF, Martinez R, Garcia-Arraras JE (1996) Galanin-like immunoreactivity in the sea cucumber Holothuria glaberrima. Cell Tissue Res 286(3):385–391CrossRefGoogle Scholar
  19. Elphick MR, Reeve JR Jr, Burke RD, Thorndyke MC (1991) Isolation of the neuropeptide SALMFamide-1 from starfish using a new antiserum. Peptides 12(3):455–459CrossRefGoogle Scholar
  20. Emson RH, Wilkie IC (1980) Fission and autotomy in echinoderms. Oceanogr Mar Biol Annu Rev 18:155–250Google Scholar
  21. Garcia-Arraras JE, Dolmatov IY (2010) Echinoderms: potential model systems for studies on muscle regeneration. Curr Pharm Des 16(8):942–955CrossRefGoogle Scholar
  22. Garcia-Arraras JE, Greenberg MJ (2001) Visceral regeneration in holothurians. Microsc Res Tech 55(6):438–451.  https://doi.org/10.1002/jemt.1189CrossRefPubMedGoogle Scholar
  23. Garcia-Arraras JE, Viruet E (1993) Enteric nerve fibers of holothurians are recognized by an antibody to acetylated alpha-tubulin. Neurosci Lett 157(2):153–156CrossRefGoogle Scholar
  24. Garcia-Arraras JE, Enamorado-Ayala I, Torres-Avillan I, Rivera V (1991a) FMRFamide-like immunoreactivity in cells and fibers of the holothurian nervous system. Neurosci Lett 132(2):199–202CrossRefGoogle Scholar
  25. Garcia-Arraras JE, Torres-Avillan I, Ortiz-Miranda S (1991b) Cells in the intestinal system of holothurians (Echinodermata) express cholecystokinin-like immunoreactivity. Gen Comp Endocrinol 83(2):233–242CrossRefGoogle Scholar
  26. Garcia-Arraras JE, Estrada-Rodgers L, Santiago R, Torres II, Diaz-Miranda L, Torres-Avillan I (1998) Cellular mechanisms of intestine regeneration in the sea cucumber, Holothuria glaberrima Selenka (Holothuroidea:Echinodermata). J Exp Zool 281(4):288–304CrossRefGoogle Scholar
  27. Garcia-Arraras JE, Rojas-Soto M, Jimenez LB, Diaz-Miranda L (2001) The enteric nervous system of echinoderms: unexpected complexity revealed by neurochemical analysis. J Exp Biol 204(Pt 5):865–873PubMedGoogle Scholar
  28. Garcia-Arraras JE, Schenk C, Rodrigues-Ramirez R, Torres II, Valentin G, Candelaria AG (2006) Spherulocytes in the echinoderm Holothuria glaberrima and their involvement in intestinal regeneration. Dev Dyn 235(12):3259–3267.  https://doi.org/10.1002/dvdy.20983CrossRefPubMedGoogle Scholar
  29. Garcia-Arraras JE, Valentin-Tirado G, Flores JE, Rosa RJ, Rivera-Cruz A, San Miguel-Ruiz JE, Tossas K (2011) Cell dedifferentiation and epithelial to mesenchymal transitions during intestinal regeneration in H. glaberrima. BMC Dev Biol 11:61.  https://doi.org/10.1186/1471-213X-11-61CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hernandez-Pasos J, Valentin-Tirado G, Garcia-Arraras JE (2017) Melanotransferrin: new homolog genes and their differential expression during intestinal regeneration in the sea cucumber Holothuria glaberrima. J Exp Zool B Mol Dev Evol 328(3):259–274.  https://doi.org/10.1002/jez.b.22731CrossRefPubMedPubMedCentralGoogle Scholar
  31. Holland LZ (2015) Evolution of basal deuterostome nervous systems. J Exp Biol 218(Pt 4):637–645.  https://doi.org/10.1242/jeb.109108CrossRefPubMedGoogle Scholar
  32. Hyman LH (1955) The invertebrates: echinodermata. McGraw-Hill, New YorkGoogle Scholar
  33. Kamenev YO, Dolmatov IY (2015) Posterior regeneration following fission in the holothurian Cladolabes schmeltzii (Dendrochirotida: Holothuroidea). Microsc Res Tech 78(7):540–552.  https://doi.org/10.1002/jemt.22507CrossRefPubMedGoogle Scholar
  34. Kamenev YO, Dolmatov IY (2017) Anterior regeneration after fission in the holothurian Cladolabes schmeltzii (Dendrochirotida: Holothuroidea). Microsc Res Tech 80(2):183–194.  https://doi.org/10.1002/jemt.22786CrossRefPubMedGoogle Scholar
  35. Kamenev YO, Dolmatov IY, Frolova LT, Khang NA (2013) The morphology of the digestive tract and respiratory organs of the holothurian Cladolabes schmeltzii (Holothuroidea, Dendrochirotida). Tissue Cell 45(2):126–139.  https://doi.org/10.1016/j.tice.2012.10.002CrossRefPubMedGoogle Scholar
  36. Kille FR (1935) Regeneration in Thyone briareus lesueur following induced autotomy. Biol Bull 69(1):82–108.  https://doi.org/10.2307/1537360CrossRefGoogle Scholar
  37. Leibson NL (1992) Regeneration of digestive tube in holothurians Stichopus japonicus and Eupentacta fraudatrix. Monogr Dev Biol 23:51–61PubMedGoogle Scholar
  38. Long KA, Nossa CW, Sewell MA, Putnam NH, Ryan JF (2016) Low coverage sequencing of three echinoderm genomes: the brittle star Ophionereis fasciata, the sea star Patiriella regularis, and the sea cucumber Australostichopus mollis. Gigascience 5:20.  https://doi.org/10.1186/s13742-016-0125-6CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mashanov VS, Garcia-Arraras JE (2011) Gut regeneration in holothurians: a snapshot of recent developments. Biol Bull 221(1):93–109.  https://doi.org/10.1086/BBLv221n1p93CrossRefPubMedGoogle Scholar
  40. Mashanov VS, Dolmatov IY, Heinzeller T (2005) Transdifferentiation in holothurian gut regeneration. Biol Bull 209(3):184–193.  https://doi.org/10.2307/3593108CrossRefPubMedGoogle Scholar
  41. Mashanov VS, Zueva OR, Heinzeller T, Dolmatov IY (2006) Ultrastructure of the circumoral nerve ring and the radial nerve cords in holothurians (Echinodermata). Zoomorphology 125:27–38CrossRefGoogle Scholar
  42. Mashanov VS, Zueva OR, Heinzeller T (2008) Regeneration of the radial nerve cord in a holothurian: a promising new model system for studying post-traumatic recovery in the adult nervous system. Tissue Cell 40(5):351–372.  https://doi.org/10.1016/j.tice.2008.03.004CrossRefPubMedGoogle Scholar
  43. Mashanov VS, Zueva OR, Heinzeller T, Aschauer B, Naumann WW, Grondona JM, Cifuentes M, Garcia-Arraras JE (2009) The central nervous system of sea cucumbers (Echinodermata: Holothuroidea) shows positive immunostaining for a chordate glial secretion. Front Zool 6:11.  https://doi.org/10.1186/1742-9994-6-11CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mashanov VS, Zueva OR, Garcia-Arraras JE (2010a) Organization of glial cells in the adult sea cucumber central nervous system. Glia 58(13):1581–1593.  https://doi.org/10.1002/glia.21031CrossRefPubMedGoogle Scholar
  45. Mashanov VS, Zueva OR, Rojas-Catagena C, Garcia-Arraras JE (2010b) Visceral regeneration in a sea cucumber involves extensive expression of survivin and mortalin homologs in the mesothelium. BMC Dev Biol 10:117.  https://doi.org/10.1186/1471-213X-10-117CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mashanov VS, Zueva OR, Garcia-Arraras JE (2012) Expression of Wnt9, TCTP, and Bmp1/Tll in sea cucumber visceral regeneration. Gene Expr Patterns 12(1–2):24–35.  https://doi.org/10.1016/j.gep.2011.10.003CrossRefPubMedGoogle Scholar
  47. Mashanov VS, Zueva OR, Garcia-Arraras JE (2013) Radial glial cells play a key role in echinoderm neural regeneration. BMC Biol 11:49.  https://doi.org/10.1186/1741-7007-11-49CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mashanov VS, Zueva O, Garcia-Arraras JE (2014a) Postembryonic organogenesis of the digestive tube: why does it occur in worms and sea cucumbers but fail in humans? Curr Top Dev Biol 108:185–216.  https://doi.org/10.1016/B978-0-12-391498-9.00006-1CrossRefPubMedPubMedCentralGoogle Scholar
  49. Mashanov VS, Zueva OR, Garcia-Arraras JE (2014b) Transcriptomic changes during regeneration of the central nervous system in an echinoderm. BMC Genomics 15:357.  https://doi.org/10.1186/1471-2164-15-357CrossRefPubMedPubMedCentralGoogle Scholar
  50. Mashanov VS, Zueva OR, Garcia-Arraras JE (2015a) Expression of pluripotency factors in echinoderm regeneration. Cell Tissue Res 359(2):521–536.  https://doi.org/10.1007/s00441-014-2040-4CrossRefPubMedGoogle Scholar
  51. Mashanov VS, Zueva OR, Garcia-Arraras JE (2015b) Heterogeneous generation of new cells in the adult echinoderm nervous system. Front Neuroanat 9:123.  https://doi.org/10.3389/fnana.2015.00123CrossRefPubMedPubMedCentralGoogle Scholar
  52. Mashanov VS, Zueva OR, Garcia-Arraras JE (2015c) Myc regulates programmed cell death and radial glia dedifferentiation after neural injury in an echinoderm. BMC Dev Biol 15:24.  https://doi.org/10.1186/s12861-015-0071-zCrossRefPubMedPubMedCentralGoogle Scholar
  53. Mashanov V, Zueva O, Rubilar T, Epherra L, García-Arrarás JE (2016) Echinodermata. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, OxfordGoogle Scholar
  54. Mashanov V, Zueva O, Mashanova D, Garcia-Arraras JE (2017a) Expression of stem cell factors in the adult sea cucumber digestive tube. Cell Tissue Res 370(3):427–440.  https://doi.org/10.1007/s00441-017-2692-yCrossRefPubMedGoogle Scholar
  55. Mashanov VS, Zueva OR, Garcia-Arraras JE (2017b) Inhibition of cell proliferation does not slow down echinoderm neural regeneration. Front Zool 14:12.  https://doi.org/10.1186/s12983-017-0196-yCrossRefPubMedPubMedCentralGoogle Scholar
  56. Mendez AT, Roig-Lopez JL, Santiago P, Santiago C, Garcia-Arraras JE (2000) Identification of Hox gene sequences in the sea cucumber Holothuria glaberrima Selenka (Holothuroidea: Echinodermata). Mar Biotechnol (NY) 2(3):231–240.  https://doi.org/10.1007/s101269900027CrossRefGoogle Scholar
  57. Mosher C (1956) Observation on evisceration and visceral regeneration in the sea cucumber Actinopyga agassizi Selenka. Zoologica (NY) 41:17–26Google Scholar
  58. Murray G, Garcia-Arraras JE (2004) Myogenesis during holothurian intestinal regeneration. Cell Tissue Res 318(3):515–524.  https://doi.org/10.1007/s00441-004-0978-3CrossRefPubMedGoogle Scholar
  59. Odintsova NA, Dolmatov IY, Mashanov VS (2005) Regenerating holothurian tissues as a source of cells for long-term cell cultures. Mar Biol 146(5):915–921.  https://doi.org/10.1007/s00227-004-1495-3CrossRefGoogle Scholar
  60. Ortiz-Pineda PA, Ramirez-Gomez F, Perez-Ortiz J, Gonzalez-Diaz S, Santiago-De Jesus F, Hernandez-Pasos J, Del Valle-Avila C, Rojas-Cartagena C, Suarez-Castillo EC, Tossas K, Mendez-Merced AT, Roig-Lopez JL, Ortiz-Zuazaga H, Garcia-Arraras JE (2009) Gene expression profiling of intestinal regeneration in the sea cucumber. BMC Genomics 10:262.  https://doi.org/10.1186/1471-2164-10-262CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pasten C, Ortiz-Pineda PA, Garcia-Arraras JE (2012a) Ubiquitin-proteasome system components are upregulated during intestinal regeneration. Genesis 50(4):350–365.  https://doi.org/10.1002/dvg.20803CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pasten C, Rosa R, Ortiz S, Gonzalez S, Garcia-Arraras JE (2012b) Characterization of proteolytic activities during intestinal regeneration of the sea cucumber, Holothuria glaberrima. Int J Dev Biol 56(9):681–691.  https://doi.org/10.1387/ijdb.113473cpCrossRefPubMedPubMedCentralGoogle Scholar
  63. Pearse AS (1909) Autotomy in holothurians. Biol Bull 18:42–49CrossRefGoogle Scholar
  64. Perseke M, Golombek A, Schlegel M, Struck TH (2013) The impact of mitochondrial genome analyses on the understanding of deuterostome phylogeny. Mol Phylogenet Evol 66(3):898–905.  https://doi.org/10.1016/j.ympev.2012.11.019CrossRefPubMedGoogle Scholar
  65. Quinones JL, Rosa R, Ruiz DL, Garcia-Arraras JE (2002) Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol 250(1):181–197CrossRefGoogle Scholar
  66. Roig-López JL, Santiago P, Jiménez B, Santiago C, García-Arrarás JE (2000) Strategies to identify differentially expressed genes during regeneration. In: Barker M (ed) Echinoderms 2000. Swelts & Zeitlinger, Lisse, pp 49–54Google Scholar
  67. Rojas-Cartagena C, Ortiz-Pineda P, Ramirez-Gomez F, Suarez-Castillo EC, Matos-Cruz V, Rodriguez C, Ortiz-Zuazaga H, Garcia-Arraras JE (2007) Distinct profiles of expressed sequence tags during intestinal regeneration in the sea cucumber Holothuria glaberrima. Physiol Genomics 31(2):203–215.  https://doi.org/10.1152/physiolgenomics.00228.2006CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rosado-Olivieri EA, Ramos-Ortiz GA, Hernandez-Pasos J, Diaz-Balzac CA, Vazquez-Rosa E, Valentin-Tirado G, Vega IE, Garcia-Arraras JE (2017) A START-domain-containing protein is a novel marker of nervous system components of the sea cucumber Holothuria glaberrima. Comp Biochem Physiol B Biochem Mol Biol 214:57–65.  https://doi.org/10.1016/j.cbpb.2017.08.004CrossRefPubMedGoogle Scholar
  69. San Miguel-Ruiz JE, Garcia-Arraras JE (2007) Common cellular events occur during wound healing and organ regeneration in the sea cucumber Holothuria glaberrima. BMC Dev Biol 7:115.  https://doi.org/10.1186/1471-213X-7-115CrossRefPubMedPubMedCentralGoogle Scholar
  70. San Miguel-Ruiz JE, Maldonado-Soto AR, Garcia-Arraras JE (2009) Regeneration of the radial nerve cord in the sea cucumber Holothuria glaberrima. BMC Dev Biol 9:3.  https://doi.org/10.1186/1471-213X-9-3CrossRefPubMedPubMedCentralGoogle Scholar
  71. Santiago P, Roig-Lopez JL, Santiago C, Garcia-Arraras JE (2000) Serum amyloid A protein in an echinoderm: its primary structure and expression during intestinal regeneration in the sea cucumber Holothuria glaberrima. J Exp Zool 288(4):335–344.  https://doi.org/10.1002/1097-010X(20001215)288:4<335::AID-JEZ6>3.0.CO;2-1CrossRefPubMedGoogle Scholar
  72. Satoh N, Rokhsar D, Rokhsar D, Nishikawa T (2014) Chordate evolution and the three-phylum system. Proc Biol Sci 281(1794):20141729.  https://doi.org/10.1098/rspb.2014.1729CrossRefPubMedPubMedCentralGoogle Scholar
  73. Shukalyuk AI, Dolmatov IY (2001) Regeneration of the digestive tube in the holothurian Apostichopus japonicus after evisceration. Russ J Mar Biol 27(3):168–173.  https://doi.org/10.1023/A:1016717502616CrossRefGoogle Scholar
  74. Smith GN Jr (1971a) Regeneration in the sea cucumber Leptosynapta. I. The process of regeneration. J Exp Zool 177(3):319–329.  https://doi.org/10.1002/jez.1401770306CrossRefPubMedGoogle Scholar
  75. Smith GN Jr (1971b) Regeneration in the sea cucumber Leptosynapta. II. The regenerative capacity. J Exp Zool 177(3):331–342.  https://doi.org/10.1002/jez.1401770307CrossRefPubMedGoogle Scholar
  76. Suarez-Castillo EC, Garcia-Arraras JE (2007) Molecular evolution of the ependymin protein family: a necessary update. BMC Evol Biol 7:23.  https://doi.org/10.1186/1471-2148-7-23CrossRefPubMedPubMedCentralGoogle Scholar
  77. Suarez-Castillo EC, Medina-Ortiz WE, Roig-Lopez JL, Garcia-Arraras JE (2004) Ependymin, a gene involved in regeneration and neuroplasticity in vertebrates, is overexpressed during regeneration in the echinoderm Holothuria glaberrima. Gene 334:133–143.  https://doi.org/10.1016/j.gene.2004.03.023CrossRefPubMedGoogle Scholar
  78. Sun L, Chen M, Yang H, Wang T, Liu B, Shu C, Gardiner DM (2011) Large scale gene expression profiling during intestine and body wall regeneration in the sea cucumber Apostichopus japonicus. Comp Biochem Physiol Part D Genomics Proteomics 6(2):195–205.  https://doi.org/10.1016/j.cbd.2011.03.002CrossRefPubMedGoogle Scholar
  79. Sun L, Yang H, Chen M, Ma D, Lin C (2013) RNA-Seq reveals dynamic changes of gene expression in key stages of intestine regeneration in the sea cucumber Apostichopus japonicus [corrected]. PLoS One 8(8):e69441.  https://doi.org/10.1371/journal.pone.0069441CrossRefPubMedPubMedCentralGoogle Scholar
  80. Tossas K, Qi-Huang S, Cuyar E, Garcia-Arraras JE (2014) Temporal and spatial analysis of enteric nervous system regeneration in the sea cucumber Holothuria glaberrima. Regeneration (Oxf) 1(3):10–26.  https://doi.org/10.1002/reg2.15CrossRefGoogle Scholar
  81. Tracey DJ (1972) Evisceration and regeneration in Thyone okeni (Bell, 1884). Proc Linnean Soc N S W 97:72–81Google Scholar
  82. 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(1):34–49.  https://doi.org/10.2307/1542802CrossRefPubMedGoogle Scholar
  83. Vazquez-Velez GE, Rodriguez-Molina JF, Quinones-Frias MC, Pagan M, Garcia-Arraras JE (2016) A proteoglycan-like molecule offers insights into ground substance changes during holothurian intestinal regeneration. J Histochem Cytochem 64(6):381–393.  https://doi.org/10.1369/0022155416645781CrossRefPubMedPubMedCentralGoogle Scholar
  84. Wilkie IC (2002) Is muscle involved in the mechanical adaptability of echinoderm mutable collagenous tissue? J Exp Biol 205(Pt 2):159–165PubMedGoogle Scholar
  85. Zhang X, Sun L, Yuan J, Sun Y, Gao Y, Zhang L, Li S, Dai H, Hamel JF, Liu C, Yu Y, Liu S, Lin W, Guo K, Jin S, Xu P, Storey KB, Huan P, Zhang T, Zhou Y, Zhang J, Lin C, Li X, Xing L, Huo D, Sun M, Wang L, Mercier A, Li F, Yang H, Xiang J (2017) The sea cucumber genome provides insights into morphological evolution and visceral regeneration. PLoS Biol 15(10):e2003790.  https://doi.org/10.1371/journal.pbio.2003790CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • José E. García-Arrarás
    • 1
  • María I. Lázaro-Peña
    • 2
  • Carlos A. Díaz-Balzac
    • 3
  1. 1.Department of BiologyUniversity of Puerto Rico - Río Piedras CampusSan JuanPuerto Rico
  2. 2.Department of Biomedical GeneticsUniversity of Rochester Medical CenterRochesterUSA
  3. 3.Department of MedicineUniversity of Rochester Medical Center, Strong Memorial HospitalRochesterUSA

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