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Cell and Tissue Research

, Volume 370, Issue 1, pp 13–28 | Cite as

An integrated view of asteroid regeneration: tissues, cells and molecules

  • Yousra Ben Khadra
  • Michela Sugni
  • Cinzia Ferrario
  • Francesco Bonasoro
  • Ana Varela Coelho
  • Pedro Martinez
  • Maria Daniela Candia Carnevali
Review

Abstract

The potential for repairing and replacing cells, tissues, organs and body parts is considered a primitive attribute of life shared by all the organisms, even though it may be expressed to a different extent and which is essential for the survival of both individual and whole species. The ability to regenerate is particularly evident and widespread within invertebrates. In spite of the wide availability of experimental models, regeneration has been comprehensively explored in only a few animal systems (i.e., hydrozoans, planarians, urodeles) leaving many other animal groups unexplored. The regenerative potential finds its maximum expression in echinoderms. Among echinoderm classes, asteroids offer an impressive range of experimental models in which to study arm regeneration at different levels. Many studies have been recently carried out in order to understand the regenerative mechanisms in asteroids and the overall morphological processes have been well documented in different starfish species, such as Asterias rubens, Leptasterias hexactis and Echinaster sepositus. In contrast, very little is known about the molecular mechanisms that control regeneration development and patterning in these models. The origin and the fate of cells involved in the regenerative process remain a matter of debate and clear insights will require the use of complementary molecular and proteomic approaches to study this problem. Here, we review the current knowledge regarding the cellular, proteomic and molecular aspects of asteroid regeneration.

Keywords

Starfish Regeneration Cell and tissue Proteomic Molecular aspects 

Abbreviations

CE

Coelomic epithelium

ECM

Extracellular matrix

EMT

Epithelial to mesenchymal transition

MCT

Mutable collagenous tissue

OPR

Ocular-plate rule

RNC

Radial nerve cord

RWC

Radial water canal

SLS

Spindle-like structure

srap

Starfish regeneration-associated protease

Notes

Acknowledgements

The authors are grateful to Dr. Arianna Daviddi and Dr. Greta Valoti for providing histological images of M. glacialis arm regeneration and E. sepositus arm explants, respectively and to Christopher Evans for English editing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Abe N, Cavalli V (2008) Nerve injury signaling. Curr Opin Neurobiol 18:276–283CrossRefPubMedPubMedCentralGoogle Scholar
  2. Agata K, Tanaka T, Kobayashi C, Kato K, Saitho Y (2003) Intercalary regeneration in planarians. Dev Dynam 226:308–316CrossRefGoogle Scholar
  3. Ambron RT, Walters ET (1996) Priming events and retrograde injury signals. Mol Neurobiol 13:61–79CrossRefPubMedGoogle Scholar
  4. Bely AE (2010) Evolutionary loss of animal regeneration: pattern and process. Integr Comp Biol 50:515–527CrossRefPubMedGoogle Scholar
  5. Ben Khadra Y, Said K, Thorndyke MC, Martinez P (2014) Homeobox genes expressed during echinoderm arm regeneration. Biochem Genet 52:166–180CrossRefPubMedGoogle Scholar
  6. Ben Khadra Y, Ferrario C, Di Benedetto C, Said K, Bonasoro F, Candia Carnevali MD, Sugni M (2015a) Wound repair during arm regeneration in the red starfish Echinaster sepositus. Wound Repair Regen 23:611–622CrossRefPubMedGoogle Scholar
  7. Ben Khadra Y, Ferrario C, Di Benedetto C, Said K, Bonasoro F, Candia Carnevali MD, Sugni M (2015b) Re-growth, morphogenesis, and differentiation during starfish arm regeneration. Wound Repair Regen 23:623–634CrossRefPubMedGoogle Scholar
  8. Biressi A, Ting Z, Dupont S, Dahlberg C, Di Benedetto C, Bonasoro F, Thorndyke MC, Candia Carnevali MD (2010) Wound-healing and arm regeneration in Ophioderma longicaudum and Amphiura filiformis (Ophiuroidea, Echinodermata): Comparative morphogenesis and histogenesis. Zoomorphology 129:1–19CrossRefGoogle Scholar
  9. Birnbaum KD, Sánchez-Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bonasoro F, Candia Carnevali MD, Moss C, Thorndyke MC (1998) Epimorphic versus morphallactic mechanisms in arm regeneration of crinoids and asteroids: pattern of cell proliferation differentiation and cell lineage. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Balkema, Rotterdam, pp 13–18Google Scholar
  11. Brockes JP, Kumar A (2008) Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 24:525–549CrossRefPubMedGoogle Scholar
  12. Candia Carnevali MD (2006) Regeneration in echinoderms: repair, re-growth and cloning. Invertebr Surviv J 3:64–76Google Scholar
  13. Candia Carnevali MD, Bonasoro F (1995) Arm regeneration and pattern formation in crinoids. In: Smith E, Campbell (eds) Echinoderm research. Balkema, Rotterdam, pp 245–253Google Scholar
  14. Candia Carnevali MD, Bonasoro F (2001a) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426CrossRefPubMedGoogle Scholar
  15. Candia Carnevali MD, Bonasoro F (2001b) Introduction to the biology of regeneration in echinoderms. Microsc Res Tech 55:365–368CrossRefPubMedGoogle Scholar
  16. Candia Carnevali MD, Burighel P (2010) Regeneration in echinoderms and ascidians. In: Encyclopedia of Life Sciences (ELS). Wiley, Chichester doi:  10.1002/9780470015902.a0022102
  17. Candia Carnevali MD, Bonasoro F, Wilkie IC (1995) Coelom and tinkering in echinoids. In: Lanzavecchia G, Valvassori R, Candia Carnevali (eds) “Body Cavities: Phylogeny and Function”. Selected Symposia and Monographs U.Z.I. 8, Mucchi, Modena, pp.135–165Google Scholar
  18. Candia Carnevali MD, Thorndyke MC, Matranga V (2009) Regenerating echinoderms: a promise to understand stem cell potential. In: Rinkevich B, Matranga V (eds) Stem cells in marine organisms. Springer, Dordrecht. doi:  10.1007/978-90-481-2767-2-7
  19. Cisternas P, Byrne M (2009) Expression of Hox4 during development of the pentamerous juvenile starfish Parvulastra exigua. Dev Genes Evol 219:613–618CrossRefPubMedGoogle Scholar
  20. Clevers H, Loh KM, Nusse R (2014) An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346(6205):1248012. doi: 10.1126/science.1248012 CrossRefPubMedGoogle Scholar
  21. Czarkwiani A, Ferrario F, Dylus DV, Sugni M, Oliveri P (2016) Skeletal regeneration in the brittle star Amphiura filiformis. Front Zool 22:13–18Google Scholar
  22. Daviddi (2015). Microscopic anatomy of arm-tip regeneration in the starfish Marthasterias glacialis (Linneaus, 1758) following traumatic amputation. Master thesis, University of MilanGoogle Scholar
  23. Di Benedetto C, Parma L, Barbaglio A, Sugni M, Bonasoro F, Candia Carnevali MD (2014) Echinoderm regeneration: an in vitro approach using the crinoid Antedon mediterranea. Cell Tissue Res 358:189–201CrossRefPubMedGoogle Scholar
  24. Dolmatov IY, Ginanova TT (2001) Muscle regeneration in holothurians. Microsc Res Tech 55:452–463CrossRefPubMedGoogle Scholar
  25. Dupont S, Thorndyke MC (2007) Bridging the regeneration gap: insights from echinoderm models. Nat Rev Genet 8:1–4CrossRefGoogle Scholar
  26. Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature. 146 doi: 10.1038/425146a
  27. Echeverri K, Tanaka EM (2005) Proximodistal patterning during limb regeneration. Dev Biol 279:391–401CrossRefPubMedGoogle Scholar
  28. Franco CF, Santos R, Coelho AV (2011a) Exploring the proteome of an echinoderm nervous system: 2DE of the sea star radial nerve cord and the synaptosomal membranes subproteome. Proteomics 11:1359–1364CrossRefPubMedGoogle Scholar
  29. Franco CF, Santos R, Coelho AV (2011b) Proteome characterization of starfish coelomocytes - the innate immune effector cells of echinoderms. Proteomics 11:3587–3592CrossRefPubMedGoogle Scholar
  30. Franco CF, Soares R, Pires E, Santos R, Coelho AV (2012) Radial nerve cord protein phosphorylation dynamics during starfish arm tip wound healing events. Electrophoresis 33:3764–3778CrossRefPubMedGoogle Scholar
  31. Franco CF, Santos R, Coelho AV (2014) Proteolytic events are relevant cellular responses during nervous system regeneration of the starfish Marthasterias glacialis. J Proteomics 99:1–25CrossRefGoogle Scholar
  32. Gabre JL, Martinez P, Sköld HN, Ortega-Martinez O, Abril JF (2015) The coelomic epithelium transcriptome from a clonal sea star, Coscinasterias muricata. Mar Genomics. doi: 10.1016/j.margen.2015.07.010 PubMedGoogle Scholar
  33. García-Arrarás JE, Dolmatov IY (2010) Echinoderms; potential model systems for studies on muscle regeneration. Curr Pharm Des 16:942–955CrossRefPubMedPubMedCentralGoogle Scholar
  34. García-Arrarás JE, Valentín-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 11:61CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gilbert SF (2000) Developmental Biology, 6th edn. Sinauer Associates, SunderlandGoogle Scholar
  36. Gorshkov AN, Blinova MI, Pinaev GP (2009) Ultrastructure of coelomic epithelium and coelomocytes of the starfish Asterias rubens L. in norm and after wounding. Cell Tissue Biol 3:477–490CrossRefGoogle Scholar
  37. Goss RJ (1969) Principles of regeneration. Academic Press, New YorkGoogle Scholar
  38. Heinzeller T, Welsch U (2001) The echinoderm nervous System and its phylogenetic interpretation. In: Roth G, Wullimann MF (eds) Brain Evolution and Cognition. Wiley, New York, pp 41–7Google Scholar
  39. Hernroth B, Farahani F, Brunborg G, Dupont S, Dejmek A, Skold H (2010) Possibility of mixed progenitor cells in sea star arm regeneration. J Exp Zool (Mol Dev Evol) 6:457–468CrossRefGoogle Scholar
  40. Holm K, Dupont S, Skold H, Stenius A, Thorndyke MC, Hernroth B (2008a) Induced cell proliferation in putative haematopoietic tissues of the sea star, Asterias rubens (L.). J Exp Biol 211:2551–2558CrossRefPubMedGoogle Scholar
  41. Holm K, Hernroth B, Thorndyke MC (2008b) Coelomocyte number and expression of HSP70 in wounded sea stars during hypoxia. Cell Tissue Res 334:319–325CrossRefPubMedGoogle Scholar
  42. Hotchkiss FHC (2009) Arm stumps and regeneration models in Asteroidea (Echinodermata). Proc Biol Soc Wash 122:342–354CrossRefGoogle Scholar
  43. Hotchkiss FHC (2012) Growth zones and extraxial-axial skeletal homologies in Asteroidea (Echinodermata). Proc Biol Soc Wash 125:106.121CrossRefGoogle Scholar
  44. Hyman LH (1955) The Invertebrates. Echinodermata, vol XIV. McGraw-Hill, New YorkGoogle Scholar
  45. Ibrahim MM, Chen L, Bond JE, Medina MA, Ren L, Kokosis G, Selim AM, Levinson H (2015) Myofibroblasts contribute to but are not necessary for wound contraction. Lab Investig 95:1429–1438CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119:1420–1428CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lawrence JM (2013) Starfish: Biology and Ecology of the Asteroidea. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  48. Lehmann WM (1951) Anomalies et régénérations chez quelques Asterozoa paléozoïques. 5ème ser. Bull Soc Géol Fr 20:267–274Google Scholar
  49. Lowe CJ, Wray GA (1997) Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718–721CrossRefPubMedGoogle Scholar
  50. Mashanov VS, García-Arrarás JE (2011) Gut regeneration in holothurians: a snapshot of recent developments. Biol Bull 221:93–109CrossRefPubMedGoogle Scholar
  51. 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
  52. 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 40:351–372CrossRefPubMedGoogle Scholar
  53. Mashanov VS, Zueva OR, Heinzeller T, Aschauer B, Naumann WW, Grondona JE, Cifuentes M, García-Arrarás JE (2009) The central nervous system of sea cucumbers (Echinodermata: Holothuroidea) shows positive immunostaining for a chordate glial secretion. Front Zool 6:11CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mashanov VS, Zueva OR, García-Arrarás JE (2010) Organization of the glial cells in the adult sea cucumber central nervous system. Glia 58:1581–1593PubMedGoogle Scholar
  55. Mashanov VS, Zueva OR, García-Arrarás JE (2013) Radial glial cells play a key role in echinoderm neural regeneration. BMC Biol 11:49–66CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mashanov VS, Zueva OR, García-Arrarás JE (2014) Transcriptomic changes during regeneration of the CNS in an echinoderm. BMC Genomics 15:357CrossRefPubMedPubMedCentralGoogle Scholar
  57. Mashanov VS, Zueva OR, García-Arrarás JE (2015) Expression of pluripotency factors in echinoderm regeneration. Cell Tissue Res 359:521–536CrossRefPubMedGoogle Scholar
  58. Millot N, Vevers HG (1955) Carotenoid pigments in the optic cushion of Marthasterias glacialis (L.). J Mar Biol Assoc UK 34:279–287CrossRefGoogle Scholar
  59. Mladenov PV, Bisgrove B, Asotra S, Burke RD (1989) Mechanisms of arm-tip regeneration in the sea star Leptasterias hexactis. Roux’s Arch Dev Biol 189:19–28CrossRefGoogle Scholar
  60. Mooi R, David B (2000) What a new model of skeletal homologies tells us about asteroid evolution. Am Zool 40:326–339Google Scholar
  61. 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 353:421–436CrossRefGoogle Scholar
  62. Motokawa T (2011) Mechanical mutability in connective tissue of starfish body wall. Biol Bull 221:280–289CrossRefPubMedGoogle Scholar
  63. Nielsen C, Martinez P (2003) Patterns of gene expression: homology or homocracy? Dev Genes Evol 213:149–154PubMedGoogle Scholar
  64. Oulhen N, Heyland A, Carrier TJ, Zazueta-Novoa V, Fresques T, Laird J, Onorato TM, Janies D, Wessel G (2016) Regeneration in bipinnaria larvae of the bat star Patiria miniata induces rapid and broad new gene expression. Mech Dev 142:10–21CrossRefPubMedPubMedCentralGoogle Scholar
  65. Pastar I, Stojadinovic O, Yin NC, Ramirez H, Nusbaum AG, Sawaya A, Patel SB, Khalid L, Isseroff RR, Tomic-Canic M (2014) Epithelialization in wound healing: a comprehensive review. Adv Wound Care 3:445–464CrossRefGoogle Scholar
  66. Patruno M, Thorndyke MC, Candia Carnevali MD, Bonasoro F, Beesley P (2001) Changes in ubiquitin conjugates and Hsp72 levels during arm regeneration in echinoderms. Mar Biotechnol 3:4–15CrossRefPubMedGoogle Scholar
  67. Pinsino A, Thorndyke MC, Matranga V (2007) Coelomocytes and post-traumatic response in the common sea star Asterias rubens. Cell Stress Chaperones 12:331–341CrossRefPubMedPubMedCentralGoogle Scholar
  68. Ramírez-Gómez F, García-Arrarás JE (2010) Echinoderm immunity. ISJ 7:211–220Google Scholar
  69. 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. doi:  10.1007/978-90-481-2767-2_4
  70. Robertson AJ, Croce J, Carbonneau S, Voronina E, Miranda E, McClay DR, Coffman JA (2006) The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Dev Biol 300:321–334CrossRefPubMedGoogle Scholar
  71. 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 7:115CrossRefPubMedPubMedCentralGoogle Scholar
  72. San Miguel-Ruiz JE, Maldonado-Soto AR, García-Arrarás JE (2009) Regeneration of the radial nerve cord in the sea cucumber Holothuria glaberrima. BMC Dev Biol 9:3CrossRefPubMedPubMedCentralGoogle Scholar
  73. Sánchez-Alvarado A, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7:873–884CrossRefPubMedGoogle Scholar
  74. Sharlaimova NS, Petukhova OA (2012) Characteristics of populations of the coelomic fluid and coelomic epithelium cells from the starfish Asterias rubens L. able attach to and spread on various substrates. Cell Tissue Biol 6:176–188CrossRefGoogle Scholar
  75. Siemerink MJ, Klaassen I, Van Noorden CJ, Schlingemann RO (2012) Endothelial tip cells in ocular angiogenesis: potential target for anti-angiogenesis therapy. J Histochem Cytochem 61:101–115CrossRefPubMedGoogle Scholar
  76. Smith LC, Davidson EH (1994) The echinoderm immune system. Ann NY Acad Sci 712:260–301CrossRefGoogle Scholar
  77. Smith LC, Chang L, Britten RJ, Davidson EH (1996) Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Immunology 156:593–602Google Scholar
  78. Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21:172–185CrossRefPubMedPubMedCentralGoogle Scholar
  79. Thorndyke MC, Chen W-C, Beesley PW, Patruno M (2001) Molecular approach to echinoderm regeneration. Microsc Res Tech 55:474–485CrossRefPubMedGoogle Scholar
  80. Tsan MF, Gao B (2004) Endogenous ligands of Toll-like receptors. J Leukoc Biol 76:514–519CrossRefPubMedGoogle Scholar
  81. Vickery MCL, Vickery MS, McClintock JB, Amsler CD (2001) 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 262:73–80CrossRefPubMedGoogle Scholar
  82. Viehweg J, Naumann WW, Olsson R (1998) Secretory radial glia in the ectoneural system of the sea star Asterias rubens (Echinodermata). Acta Zool 79:119–131CrossRefGoogle Scholar
  83. Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835PubMedGoogle Scholar
  84. Wilkie IC (2001) Autotomy as a prelude to regeneration in echinoderms. Microsc Res Tech 55:369–396CrossRefPubMedGoogle Scholar
  85. Wilkie IC (2005) Mutable Collagenous Tissue: overview and biotechnological perspective. In: Matranga V (ed) Echinodermata. Progress in molecular and subcellular biology. Marine molecular biotechnology. Springer, Berlin, pp 221–250Google Scholar
  86. Wilkie IC, Griffiths GVR, Glennie SF (1990) Morphological and physiological aspects of the autotomy plane in the aboral integument of Asterias rubens L. (Echinodermata). In: De Ridder C, Dubois P, LaHaye MC, Jangoux M (eds) Echinoderm research. Balkema, Rotterdam, pp 301–313Google Scholar
  87. Wolf JH, Bhatti TR, Fouraschen S, Chakravorty S, Wang L, Kurian S, Salomon D, Olthoff KM, Hancock WW, Levine MH (2014) Heat shock protein-70 is required for optimal liver regeneration after partial hepatectomy in mice. Liver Transpl 20(3):376–385CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Yousra Ben Khadra
    • 1
  • Michela Sugni
    • 2
  • Cinzia Ferrario
    • 2
  • Francesco Bonasoro
    • 2
  • Ana Varela Coelho
    • 3
  • Pedro Martinez
    • 4
    • 5
  • Maria Daniela Candia Carnevali
    • 2
  1. 1.Laboratory of Genetics, Biodiversity and Valorization of Bioresources, Higher Institute of BiotechnologyUniversity of MonastirMonastirTunisia
  2. 2.Department of BiosciencesUniversity of MilanMilanItaly
  3. 3.Instituto de Tecnologia Química e BiológicaUniversidade Nova de LisboaOeirasPortugal
  4. 4.Institut Català de Recerca i EstudisAvancats (ICREA)BarcelonaSpain
  5. 5.Genetics DepartmentUniversity of BarcelonaBarcelonaSpain

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