An evo-devo perspective on the regeneration patterns of continuous arm structures in stellate echinoderms

Abstract Regeneration is a post-embryonic developmental process common in Metazoa, which, despite obvious taxa-specific differences, can often share common principles and patterns. Among these, the distalization and (proximal) intercalation model successfully describes most animal regeneration phenomena. Stellate echinoderms (Crinoidea, Asteroidea, and Ophiuroidea) are particularly practical models for regeneration studies as the proximo-distal regrowth of their “segmental” arms, including the inner “continuous” yet homologous structures, i.e. radial water canal, radial nerve cord, and somatocoel, provide a unique opportunity to investigate the existence of evolutionarily shared regenerative patterns. In the present work, we comparatively examined the anatomy of arm regeneration in four stellate echinoderm species – the crinoid Antedon mediterranea, the asteroids Echinaster sepositus and Coscinasterias tenuispina, and the ophiuroid Amphipholis squamata. We observed that in all the models the distal elements, i.e. the apical blastema of crinoids, and terminal ossicle and tube foot of asteroids and ophiuroids, form in an early stage, followed by the proximal region, which develops in the proximal-to-distal direction. In all arms, the continuous structures develop before discrete lateral structures (e.g. ossicles and tube feet), and appear to provide materials that make the subsequent development possible. Overall, the model inferred from our study is compatible with those previously proposed for other animal models that involve processes of distalization and intercalation. The evidence of shared patterns suggests that at least some overall regeneration mechanisms have ancient origins and are well conserved throughout echinoderm and animal evolution. This study could help shed light on those evolutionarily conserved principles (patterns) among metazoan regeneration.

[1]  J. García-Arrarás,et al.  Regeneration in Echinoderms: Molecular Advancements , 2021, Frontiers in Cell and Developmental Biology.

[2]  A. Spagnuolo,et al.  A pan‐metazoan concept for adult stem cells: the wobbling Penrose landscape , 2021, Biological reviews of the Cambridge Philosophical Society.

[3]  Rui Gardner,et al.  Characterization of Coelomic Fluid Cell Types in the Starfish Marthasterias glacialis Using a Flow Cytometry/Imaging Combined Approach , 2021, Frontiers in Immunology.

[4]  G. Sukhikh,et al.  Evolution of Regeneration in Animals: A Tangled Story , 2021, Frontiers in Ecology and Evolution.

[5]  I. Dolmatov Molecular Aspects of Regeneration Mechanisms in Holothurians , 2021, Genes.

[6]  Pierre Kerner,et al.  Animal regeneration in the era of transcriptomics , 2021, Cellular and Molecular Life Sciences.

[7]  P. Oliveri,et al.  Ultrastructural and molecular analysis of the origin and differentiation of cells mediating brittle star skeletal regeneration , 2021, BMC Biology.

[8]  I. Dolmatov Variability of Regeneration Mechanisms in Echinoderms , 2020, Russian Journal of Marine Biology.

[9]  Ildikó M. L. Somorjai,et al.  Beyond Adult Stem Cells: Dedifferentiation as a Unifying Mechanism Underlying Regeneration in Invertebrate Deuterostomes , 2020, Frontiers in Cell and Developmental Biology.

[10]  M. Byrne The Link between Autotomy and CNS Regeneration: Echinoderms as Non-Model Species for Regenerative Biology. , 2020, BioEssays : news and reviews in molecular, cellular and developmental biology.

[11]  J. García-Arrarás,et al.  The nervous system component of the mesentery of the sea cucumber Holothuria glaberrima in normal and regenerating animals , 2019, Cell and Tissue Research.

[12]  M. Averof,et al.  The multifaceted role of nerves in animal regeneration. , 2019, Current opinion in genetics & development.

[13]  K. Kocot,et al.  Revisiting metazoan phylogeny with genomic sampling of all phyla , 2019, Proceedings of the Royal Society B.

[14]  Kimberly Johnson,et al.  Common themes in tetrapod appendage regeneration: a cellular perspective , 2019, EvoDevo.

[15]  M. Byrne,et al.  Expression of the neuropeptide SALMFamide-1 during regeneration of the seastar radial nerve cord following arm autotomy , 2019, Proceedings of the Royal Society B.

[16]  J. Maienschein,et al.  Understanding regeneration at different scales , 2019, eLife.

[17]  J. Coffman Regenerative Potential Across Species: An Eco-Evo-Devo Perspective , 2019, Epigenetics and Regeneration.

[18]  A. Martinez Arias,et al.  On the nature and function of organizers , 2018, Development.

[19]  A. Aboobaker,et al.  EvoRegen in animals: Time to uncover deep conservation or convergence of adult stem cell evolution and regenerative processes. , 2018, Developmental biology.

[20]  P. Oliveri,et al.  Fundamental aspects of arm repair phase in two echinoderm models. , 2018, Developmental biology.

[21]  G. Wray,et al.  Expression of genes and proteins of the pax‐six‐eya‐dach network in the metamorphic sea urchin: Insights into development of the enigmatic echinoderm body plan and sensory structures , 2018, Developmental dynamics : an official publication of the American Association of Anatomists.

[22]  Katherine M. Buckley,et al.  Echinodermata: The Complex Immune System in Echinoderms , 2018 .

[23]  P. Oliveri,et al.  Regeneration in Stellate Echinoderms: Crinoidea, Asteroidea and Ophiuroidea. , 2018, Results and problems in cell differentiation.

[24]  P. Martinez,et al.  An integrated view of asteroid regeneration: tissues, cells and molecules , 2017, Cell and Tissue Research.

[25]  E. Tanaka The Molecular and Cellular Choreography of Appendage Regeneration , 2016, Cell.

[26]  P. Oliveri,et al.  Skeletal regeneration in the brittle star Amphiura filiformis , 2016, Frontiers in Zoology.

[27]  T. Artois,et al.  Do you have the nerves to regenerate? The importance of neural signalling in the regeneration process. , 2016, Developmental biology.

[28]  C. di Benedetto,et al.  Wound repair during arm regeneration in the red starfish Echinaster sepositus , 2015, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[29]  Yousra Ben Khadra,et al.  Re‐growth, morphogenesis, and differentiation during starfish arm regeneration , 2015, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[30]  B. David,et al.  How Hox genes can shed light on the place of echinoderms among the deuterostomes , 2014, EvoDevo.

[31]  P. Martinez,et al.  Homeobox Genes Expressed During Echinoderm Arm Regeneration , 2014, Biochemical Genetics.

[32]  Olga R. Zueva,et al.  Radial glial cells play a key role in echinoderm neural regeneration , 2013, BMC Biology.

[33]  K. Kočí,et al.  Understanding regeneration through proteomics , 2013, Proteomics.

[34]  G. Boxshall,et al.  Arthropod Biology and Evolution: Molecules, Development, Morphology , 2013 .

[35]  Anoop Kumar,et al.  Nerve dependence in tissue, organ, and appendage regeneration , 2012, Trends in Neurosciences.

[36]  A. Stier,et al.  The influence of fundamental traits on mechanisms controlling appendage regeneration , 2012, Biological reviews of the Cambridge Philosophical Society.

[37]  Yishi Jin,et al.  Axon Regeneration Pathways Identified by Systematic Genetic Screening in C. elegans , 2011, Neuron.

[38]  T. Fan,et al.  Patterns and cellular mechanisms of arm regeneration in adult starfish Asterias rollestoni bell , 2011 .

[39]  P. Reddien,et al.  The cellular basis for animal regeneration. , 2011, Developmental cell.

[40]  D. Gardiner,et al.  Large scale gene expression profiling during intestine and body wall regeneration in the sea cucumber Apostichopus japonicus. , 2011, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[41]  A. Bely,et al.  Evolution of animal regeneration: re-emergence of a field. , 2010, Trends in ecology & evolution.

[42]  M. Thorndyke,et al.  Wound healing and arm regeneration in Ophioderma longicaudum and Amphiura filiformis (Ophiuroidea, Echinodermata): comparative morphogenesis and histogenesis , 2010, Zoomorphology.

[43]  G. Pinaev,et al.  Ultrastructure of coelomic epithelium and coelomocytes of the starfish Asterias rubens L. in norm and after wounding , 2009, Cell and Tissue Biology.

[44]  P. Burighel,et al.  New evidence of serotonin involvement in the neurohumoral control of crinoid arm regeneration: effects of parachlorophenylanine and methiothepin , 2009, Journal of the Marine Biological Association of the United Kingdom.

[45]  A. Perkins,et al.  Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. , 2009, Genome research.

[46]  Oleg Simakov,et al.  Multiple Wnts are involved in Hydra organizer formation and regeneration. , 2009, Developmental biology.

[47]  Anoop Kumar,et al.  The Immunoglobulin-Like Cell Adhesion Molecule Nectin and Its Associated Protein , 2011 .

[48]  Anoop Kumar,et al.  Molecular Basis for the Nerve Dependence of Limb Regeneration in an Adult Vertebrate , 2007, Science.

[49]  Denis Duboule,et al.  The rise and fall of Hox gene clusters , 2007, Development.

[50]  K. Agata,et al.  Unifying principles of regeneration I: Epimorphosis versus morphallaxis , 2007, Development, growth & differentiation.

[51]  A. Graham,et al.  Coelomic expression of a novel bone morphogenetic protein in regenerating arms of the brittle star Amphiura filiformis , 2007, Development Genes and Evolution.

[52]  M. D. Candia Carnevali,et al.  Regeneration in Echinoderms: repair, regrowth, cloning , 2006 .

[53]  G. Wray,et al.  Arrays in rays: terminal addition in echinoderms and its correlation with gene expression , 2005, Evolution & development.

[54]  M. Byrne,et al.  Engrailed is expressed in larval development and in the radial nervous system of Patiriella sea stars , 2005, Development Genes and Evolution.

[55]  J. Pérez-Pomares,et al.  The origin of the endothelial cells: an evo‐devo approach for the invertebrate/vertebrate transition of the circulatory system , 2005, Evolution & development.

[56]  Paramvir S. Dehal,et al.  Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate , 2005, PLoS biology.

[57]  M. Thorndyke,et al.  Coelomocytes and post-traumatic response in the common sea star Asterias rubens. , 2005, Cell stress & chaperones.

[58]  Robert D. Burke,et al.  Mechanisms of arm-tip regeneration in the sea star, Leptasterias hexactis , 1989, Roux's archives of developmental biology.

[59]  R. Rieger,et al.  Ultrastructure of coelomic lining in echinoderm podia: significance for concepts in the evolution of muscle and peritoneal cells , 1987, Zoomorphology.

[60]  E. Ruppert,et al.  Morphology of metazoan circulatory systems , 1983, Zoomorphology.

[61]  Y. Saitoh,et al.  Intercalary regeneration in planarians , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[62]  J. García-Arrarás,et al.  Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. , 2002, Developmental biology.

[63]  Francesco Bonasoro,et al.  Microscopic overview of crinoid regeneration , 2001, Microscopy research and technique.

[64]  M. Thorndyke,et al.  Regeneration neurohormones and growth factors in echinoderms , 2001 .

[65]  E. Davidson,et al.  Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. , 2000, Development.

[66]  Alejandro Sánchez Alvarado,et al.  Regeneration in the metazoans: why does it happen? , 2000 .

[67]  A. Meyer,et al.  Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. , 1999, Current opinion in cell biology.

[68]  M. C. Thorndyke,et al.  Cellular and molecular mechanisms of arm regeneration in crinoid echinoderms: the potential of arm explants , 1998, Development Genes and Evolution.

[69]  J E García-Arrarás,et al.  Cellular mechanisms of intestine regeneration in the sea cucumber, Holothuria glaberrima Selenka (Holothuroidea:Echinodermata). , 1998, The Journal of experimental zoology.

[70]  Patrizia Ferretti,et al.  Cellular and Molecular Basis of Regeneration: From Invertebrates to Humans , 1998 .

[71]  M. Thorndyke,et al.  Patterns of bromodeoxyuridine incorporation and neuropeptide immunoreactivity during arm regeneration in the starfish Asterias rubens , 1998 .

[72]  S. Carroll,et al.  The origin and evolution of animal appendages. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Mattias Sköld,et al.  Arm regeneration frequency in eight species of ophiuroidea (Echinodermata) from European sea areas , 1996 .

[74]  M. Daniela Candia Carnevali,et al.  Pattern of cell proliferation in the early stages of arm regeneration in the feather star Antedon mediterranea , 1995 .

[75]  B. Rinkevich,et al.  Whole-body protochordate regeneration from totipotent blood cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[76]  M. Daniela Candia Carnevali,et al.  Mechanisms of arm regeneration in the feather star Antedon mediterranea: Healing of wound and early stages of development , 1993 .

[77]  A. Fontaine,et al.  A decalification method for ultrastructure of echinoderm tissues. , 1975, Stain technology.

[78]  Ruth E. Hartley,et al.  An integrated view. , 1973 .

[79]  K. Tweedell REGENERATION OF THE ENTEROPNEUST, SACCOGLOSSUS KOWALEVSKII , 1961 .

[80]  N. B. Eales,et al.  Invertebrates , 2003 .

[81]  M. Milligan Trichrome stain for formalin-fixed tissue. , 1946, American journal of clinical pathology.

[82]  C. Dawydoff Beobachtungen über den Regenerationsprozess bei den Enteropneusten , 1909 .