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

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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.

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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

References

  • Abe N, Cavalli V (2008) Nerve injury signaling. Curr Opin Neurobiol 18:276–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ambron RT, Walters ET (1996) Priming events and retrograde injury signals. Mol Neurobiol 13:61–79

    Article  CAS  PubMed  Google Scholar 

  • Bely AE (2010) Evolutionary loss of animal regeneration: pattern and process. Integr Comp Biol 50:515–527

    Article  PubMed  Google Scholar 

  • Ben Khadra Y, Said K, Thorndyke MC, Martinez P (2014) Homeobox genes expressed during echinoderm arm regeneration. Biochem Genet 52:166–180

    Article  CAS  PubMed  Google Scholar 

  • 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 23:611–622

    Article  PubMed  Google Scholar 

  • 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 23:623–634

    Article  PubMed  Google Scholar 

  • 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 129:1–19

    Article  Google Scholar 

  • Birnbaum KD, Sánchez-Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13–18

    Google Scholar 

  • Brockes JP, Kumar A (2008) Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 24:525–549

    Article  CAS  PubMed  Google Scholar 

  • Candia Carnevali MD (2006) Regeneration in echinoderms: repair, re-growth and cloning. Invertebr Surviv J 3:64–76

    Google Scholar 

  • Candia Carnevali MD, Bonasoro F (1995) Arm regeneration and pattern formation in crinoids. In: Smith E, Campbell (eds) Echinoderm research. Balkema, Rotterdam, pp 245–253

    Google Scholar 

  • Candia Carnevali MD, Bonasoro F (2001a) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426

    Article  CAS  PubMed  Google Scholar 

  • Candia Carnevali MD, Bonasoro F (2001b) Introduction to the biology of regeneration in echinoderms. Microsc Res Tech 55:365–368

    Article  CAS  PubMed  Google Scholar 

  • Candia Carnevali MD, Burighel P (2010) Regeneration in echinoderms and ascidians. In: Encyclopedia of Life Sciences (ELS). Wiley, Chichester doi: 10.1002/9780470015902.a0022102

  • 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.135–165

  • 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

  • Cisternas P, Byrne M (2009) Expression of Hox4 during development of the pentamerous juvenile starfish Parvulastra exigua. Dev Genes Evol 219:613–618

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Czarkwiani A, Ferrario F, Dylus DV, Sugni M, Oliveri P (2016) Skeletal regeneration in the brittle star Amphiura filiformis. Front Zool 22:13–18

    Google Scholar 

  • Daviddi (2015). Microscopic anatomy of arm-tip regeneration in the starfish Marthasterias glacialis (Linneaus, 1758) following traumatic amputation. Master thesis, University of Milan

  • 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 358:189–201

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dupont S, Thorndyke MC (2007) Bridging the regeneration gap: insights from echinoderm models. Nat Rev Genet 8:1–4

    Article  Google Scholar 

  • Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature. 146 doi:10.1038/425146a

  • Echeverri K, Tanaka EM (2005) Proximodistal patterning during limb regeneration. Dev Biol 279:391–401

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1359–1364

    Article  CAS  PubMed  Google Scholar 

  • Franco CF, Santos R, Coelho AV (2011b) Proteome characterization of starfish coelomocytes - the innate immune effector cells of echinoderms. Proteomics 11:3587–3592

    Article  CAS  PubMed  Google Scholar 

  • 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 33:3764–3778

    Article  CAS  PubMed  Google Scholar 

  • Franco CF, Santos R, Coelho AV (2014) Proteolytic events are relevant cellular responses during nervous system regeneration of the starfish Marthasterias glacialis. J Proteomics 99:1–25

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • García-Arrarás JE, Dolmatov IY (2010) Echinoderms; potential model systems for studies on muscle regeneration. Curr Pharm Des 16:942–955

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 11:61

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilbert SF (2000) Developmental Biology, 6th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • 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 3:477–490

    Article  Google Scholar 

  • Goss RJ (1969) Principles of regeneration. Academic Press, New York

    Google Scholar 

  • 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 41–7

  • 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) 6:457–468

    Article  Google Scholar 

  • 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 211:2551–2558

    Article  PubMed  Google Scholar 

  • Holm K, Hernroth B, Thorndyke MC (2008b) Coelomocyte number and expression of HSP70 in wounded sea stars during hypoxia. Cell Tissue Res 334:319–325

    Article  CAS  PubMed  Google Scholar 

  • Hotchkiss FHC (2009) Arm stumps and regeneration models in Asteroidea (Echinodermata). Proc Biol Soc Wash 122:342–354

    Article  Google Scholar 

  • Hotchkiss FHC (2012) Growth zones and extraxial-axial skeletal homologies in Asteroidea (Echinodermata). Proc Biol Soc Wash 125:106.121

    Article  Google Scholar 

  • Hyman LH (1955) The Invertebrates. Echinodermata, vol XIV. McGraw-Hill, New York

    Google Scholar 

  • 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 95:1429–1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119:1420–1428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrence JM (2013) Starfish: Biology and Ecology of the Asteroidea. The Johns Hopkins University Press, Baltimore

  • Lehmann WM (1951) Anomalies et régénérations chez quelques Asterozoa paléozoïques. 5ème ser. Bull Soc Géol Fr 20:267–274

    Google Scholar 

  • Lowe CJ, Wray GA (1997) Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718–721

    Article  CAS  PubMed  Google Scholar 

  • Mashanov VS, García-Arrarás JE (2011) Gut regeneration in holothurians: a snapshot of recent developments. Biol Bull 221:93–109

    Article  CAS  PubMed  Google Scholar 

  • Mashanov VS, Zueva OR, Heinzeller T, Dolmatov IY (2006) Ultrastructure of the circumoral nerve ring and the radial nerve cords in holothurians (Echinodermata). Zoomorphology 125:27–38

    Article  Google Scholar 

  • 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 40:351–372

    Article  PubMed  Google Scholar 

  • 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 6:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2010) Organization of the glial cells in the adult sea cucumber central nervous system. Glia 58:1581–1593

    PubMed  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2013) Radial glial cells play a key role in echinoderm neural regeneration. BMC Biol 11:49–66

    Article  PubMed  PubMed Central  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2014) Transcriptomic changes during regeneration of the CNS in an echinoderm. BMC Genomics 15:357

    Article  PubMed  PubMed Central  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2015) Expression of pluripotency factors in echinoderm regeneration. Cell Tissue Res 359:521–536

    Article  CAS  PubMed  Google Scholar 

  • Millot N, Vevers HG (1955) Carotenoid pigments in the optic cushion of Marthasterias glacialis (L.). J Mar Biol Assoc UK 34:279–287

    Article  Google Scholar 

  • 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 189:19–28

    Article  Google Scholar 

  • Mooi R, David B (2000) What a new model of skeletal homologies tells us about asteroid evolution. Am Zool 40:326–339

    Google Scholar 

  • 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 353:421–436

    Article  CAS  Google Scholar 

  • Motokawa T (2011) Mechanical mutability in connective tissue of starfish body wall. Biol Bull 221:280–289

    Article  PubMed  Google Scholar 

  • Nielsen C, Martinez P (2003) Patterns of gene expression: homology or homocracy? Dev Genes Evol 213:149–154

    PubMed  Google Scholar 

  • 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 142:10–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:445–464

    Article  Google Scholar 

  • 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 3:4–15

    Article  CAS  PubMed  Google Scholar 

  • Pinsino A, Thorndyke MC, Matranga V (2007) Coelomocytes and post-traumatic response in the common sea star Asterias rubens. Cell Stress Chaperones 12:331–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramírez-Gómez F, García-Arrarás JE (2010) Echinoderm immunity. ISJ 7:211–220

    Google Scholar 

  • 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

  • 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 300:321–334

    Article  CAS  PubMed  Google Scholar 

  • 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 7:115

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 9:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Alvarado A, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7:873–884

    Article  PubMed  Google Scholar 

  • 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 6:176–188

    Article  Google Scholar 

  • 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 61:101–115

    Article  PubMed  Google Scholar 

  • Smith LC, Davidson EH (1994) The echinoderm immune system. Ann NY Acad Sci 712:260–301

    Article  Google Scholar 

  • Smith LC, Chang L, Britten RJ, Davidson EH (1996) Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Immunology 156:593–602

    CAS  Google Scholar 

  • Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21:172–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thorndyke MC, Chen W-C, Beesley PW, Patruno M (2001) Molecular approach to echinoderm regeneration. Microsc Res Tech 55:474–485

    Article  CAS  PubMed  Google Scholar 

  • Tsan MF, Gao B (2004) Endogenous ligands of Toll-like receptors. J Leukoc Biol 76:514–519

    Article  CAS  PubMed  Google Scholar 

  • 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 262:73–80

    Article  CAS  PubMed  Google Scholar 

  • Viehweg J, Naumann WW, Olsson R (1998) Secretory radial glia in the ectoneural system of the sea star Asterias rubens (Echinodermata). Acta Zool 79:119–131

    Article  Google Scholar 

  • Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835

    CAS  PubMed  Google Scholar 

  • Wilkie IC (2001) Autotomy as a prelude to regeneration in echinoderms. Microsc Res Tech 55:369–396

    Article  CAS  PubMed  Google Scholar 

  • 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 221–250

    Google Scholar 

  • 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 301–313

    Google Scholar 

  • 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):376–385

    Article  PubMed  PubMed Central  Google Scholar 

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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.

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Authors and Affiliations

  1. Laboratory of Genetics, Biodiversity and Valorization of Bioresources, Higher Institute of Biotechnology, University of Monastir, Monastir, Tunisia

    Yousra Ben Khadra

  2. Department of Biosciences, University of Milan, Milan, Italy

    Michela Sugni, Cinzia Ferrario, Francesco Bonasoro & Maria Daniela Candia Carnevali

  3. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal

    Ana Varela Coelho

  4. Institut Català de Recerca i EstudisAvancats (ICREA), Barcelona, Spain

    Pedro Martinez

  5. Genetics Department, University of Barcelona, Av. Diagonal 645, 08028, Barcelona, Spain

    Pedro Martinez

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  1. Yousra Ben Khadra
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  2. Michela Sugni
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  3. Cinzia Ferrario
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  7. Maria Daniela Candia Carnevali
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Correspondence to Michela Sugni.

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Ben Khadra, Y., Sugni, M., Ferrario, C. et al. An integrated view of asteroid regeneration: tissues, cells and molecules. Cell Tissue Res 370, 13–28 (2017). https://doi.org/10.1007/s00441-017-2589-9

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