Regulation of dorso‐ventral polarity by the nerve cord during annelid regeneration: A review of experimental evidence

Abstract An important goal for understanding regeneration is determining how polarity is conferred to the regenerate. Here we review findings in two groups of polychaete annelids that implicate the ventral nerve cord in assigning dorso‐ventral polarity, and specifically ventral identity, to the regenerate. In nereids, surgical manipulations indicate that parapodia develop where dorsal and ventral body wall territories contact. Without a nerve cord at the wound site, the regenerate differentiates no evident polarity (with no parapodia) and only dorsal identity, while with two nerve cords the regenerate develops a twinned dorso‐ventral axis (with four parapodia per segment instead of the normal two). In sabellids, a striking natural dorso‐ventral inversion in parapodial morphology occurs along the body axis and this inversion is morphologically correlated with the position of the nerve cord. Parapodial inversion also occurs in segments in which the nerve cord has been removed, even without any segment amputation. Together, these data strongly support a role for the nerve cord in annelid dorso‐ventral pattern regulation, with the nerve cord conferring ventral identity.

• Publication year

  2017

• Venue

  Regeneration

• Publication date

  2017-04-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1002/reg2.78PMID 28616245PMCID 5469730
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Regulation of dorso‐ventral polarity by the nerve cord during annelid regeneration: A review of experimental evidence

  2017cited by this paper
• Annelid models I: Capitella teleta.

  2016cited by this paper
• Mollusc models I. The snail Ilyanassa.

  2016cited by this paper
• BLOC-1 Brings Together the Actin and Microtubule Cytoskeletons to Generate Recycling Endosomes.

  2016cited by this paper
• Do you have the nerves to regenerate? The importance of neural signalling in the regeneration process.

  2016cited by this paper
• Developmental and molecular biology of annelid regeneration: a comparative review of recent studies.

  2016cited by this paper
• Phylogenetic distribution of regeneration and asexual reproduction in Annelida: regeneration is ancestral and fission evolves in regenerative clades

  2016influential reference
• Dpp/BMP2-4 Mediates Signaling from the D-Quadrant Organizer in a Spiralian Embryo.

  2016cited by this paper
• Towards a systems-level understanding of development in the marine annelid Platynereis dumerilii.

  2016cited by this paper
• Temporally coordinated signals progressively pattern the anteroposterior and dorsoventral body axes.

  2015cited by this paper
• Positional information in axolotl and mouse limb extracellular matrix is mediated via heparan sulfate and fibroblast growth factor during limb regeneration in the axolotl (Ambystoma mexicanum)

  2015cited by this paper
• Evolutionary Aspects of Annelid Regeneration

  2015cited by this paper
• Early events in annelid regeneration: a cellular perspective.

  2014cited by this paper
• Genetic and Genomic Tools for the Marine Annelid Platynereis dumerilii

  2014cited by this paper
• Report tion Is Controlled by Wnt and Bmp-Admp Signaling

  2014influential reference
• Regeneration in spiralians: evolutionary patterns and developmental processes.

  2014influential reference
• Variation in spiralian development: insights from polychaetes.

  2014cited by this paper
• An organizing activity is required for head patterning and cell fate specification in the polychaete annelid Capitella teleta: new insights into cell-cell signaling in Lophotrochozoa.

  2013cited by this paper
• Nerve dependence in tissue, organ, and appendage regeneration.

  2012cited by this paper
• Regional differences in BMP-dependence of dorsoventral patterning in the leech Helobdella.

  2012cited by this paper
• Morphological comparison of the regeneration process in Sabella spallanzanii and Branchiomma luctuosum (Annelida, Sabellida)

  2012cited by this paper
• Evolutionary crossroads in developmental biology: annelids

  2012cited by this paper
• Phylogenomic analyses unravel annelid evolution

  2011influential reference
• The evolution of dorsal-ventral patterning mechanisms in insects.

  2011cited by this paper
• Noggin and noggin-like genes control dorsoventral axis regeneration in planarians.

  2011influential reference
• A new molecular logic for BMP-mediated dorsoventral patterning in the leech Helobdella.

  2011cited by this paper
• A Bmp/Admp regulatory circuit controls maintenance and regeneration of dorsal-ventral polarity in planarians.

  2011influential reference
• Secondary embryonic axis formation by transplantation of D quadrant micromeres in an oligochaete annelid

  2011cited by this paper
• Evolution of animal regeneration: re-emergence of a field.

  2010cited by this paper
• EvoD/Vo: the origins of BMP signalling in the neuroectoderm

  2008cited by this paper
• Comparative aspects of animal regeneration.

  2008cited by this paper
• Evo-devo: variations on ancestral themes.

  2008cited by this paper
• Dscam-mediated cell recognition regulates neural circuit formation.

  2008cited by this paper
• Molecular and Cellular Basis of Regeneration and Tissue Repair

  2007cited by this paper
• Bone morphogenetic protein is required for dorso‐ventral patterning in the planarian Dugesia japonica

  2007cited by this paper
• The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians.

  2007cited by this paper
• Molecular and Cellular Basis of Regeneration and Tissue Repair

  2007cited by this paper
• BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration

  2007cited by this paper
• Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution

  2006cited by this paper
• Distribution of segment regeneration ability in the Annelida.

  2006cited by this paper
• Polychaete nervous systems: Ground pattern and variations--cLS microscopy and the importance of novel characteristics in phylogenetic analysis.

  2006cited by this paper
• Morphology of the nervous system of Polychaeta (Annelida)

  2005cited by this paper
• The ventral nerve cord signals positional information during segment formation in an annelid (Ophryotrocha puerilis, Polychaeta)

  2004cited by this paper
• A stepwise model system for limb regeneration.

  2004cited by this paper
• Dorsal and ventral positional cues required for the onset of planarian regeneration may reside in differentiated cells.

  2001cited by this paper
• The role of dorsoventral interaction in the onset of planarian regeneration.

  1999cited by this paper
• A common plan for dorsoventral patterning in Bilateria

  1996cited by this paper
• Conservation of dorsal-ventral patterning in arthropods and chordates.

  1996cited by this paper
• Cell interactions and regeneration control.

  1990cited by this paper
• Behaviour, Setal Inversion and Phylogeny of Sabellida (Polychaeta)

  1981cited by this paper
• Distal regeneration and symmetry.

  1981cited by this paper
• On the structure and homologues of the anterior end of the polychaete families sabellidae and serpulidae

  1980cited by this paper
• Induced segmental reorganization in sabellid worms.

  1978influential reference
• FUNCTIONAL MORPHOLOGY AND DEVELOPMENT OF SEGMENTAL INVERSION IN SABELLID POLYCHAETES

  1977influential reference
• [Demonstration of the dorsal character of the body wall of the aneurogenic regenerate of Nereis pelagica L. (Annelida, Polychaeta)].

  1976cited by this paper
• The effects of rotation and positional change of stump tissues upon morphogenesis of the regenerating axolotl limb.

  1975cited by this paper
• [Caudal regeneration in the presence of a supplemental nerve cord grafted dorsally in Nereis pelagica L. (Annelida Polychaeta)].

  1975cited by this paper
• Données morphologiques et anatomiques sur quelques cas de dédoublement chez les Nereidae: Interprétation morphogénétique

  1975influential reference
• Morphogenetic interactions between rotated skin cuffs and underlying stump tissues in regenerating axolotl forelimbs.

  1974cited by this paper
• [The role of brain on caudal regeneration ofNereis diversicolor O. F. Müller (Annelida polychaeta)].

  1974cited by this paper
• Mode d'action du cerveau sur la régénération caudale deNereis diversicolor O.F. Müller (Annélide Polychète)

  1974influential reference
• Induction d'une queue et de parapodes surnuméraires par déviation de l'intestin chez les Nereidae (Annélides Polychètes)

  1973cited by this paper
• [Supernumerary tail and parapodia induction by deviation of the intestine in nereids (Annelida: Polychaeta) (author's transl)].

  1973cited by this paper
• Differenciation aneurale de papilles pygidiales chez une Heteronereis (Nereis pelagica L., annelide polychete)

  1972cited by this paper
• [On the determinism of secondary sex characteristics in Nereis pelagica (Annelida polycheta)].

  1969cited by this paper
• Positional information and the spatial pattern of cellular differentiation.

  1969cited by this paper
• Origine des cellules régénératrices chezNereis diversicolor O. F. Müller (Annélide Polychète)

  1969cited by this paper
• Studies on Transplantation

  1967cited by this paper
• [Histological conditions of regeneration in the annelide Magalia perarmata Marion and Bobr].

  1960cited by this paper
• The nervous anatomy of the body segments of nereid polychaetes

  1957cited by this paper
• [Regeneration of Annelida Pterosyllis formosa Clap].

  1952cited by this paper
• Regeneration in Sabella pavonina (Sav.) and other sabellid worms

  1931cited by this paper
• Studies on Transplantation in Planaria

  1929cited by this paper

• Variations in cell plasticity and proliferation underlie distinct modes of regeneration along the antero-posterior axis in the annelid Platynereis.

  2024cites this paper
• Secondary‐tail formation during stolonization in the Japanese green syllid, Megasyllis nipponica

  2024cites this paper
• Nerves and availability of mesodermal cells are essential for the function of the segment addition zone (SAZ) during segment regeneration in polychaete annelids

  2024cites this paper
• The sea spider Pycnogonum litorale overturns the paradigm of the absence of axial regeneration in molting animals

  2023cites this paper
• Regeneration and regengrow in multicellular animals derive from the presence of processes of organ metamorphosis and continuous growth in their life cycles

  2023cites this paper
• Antero-posterior gradients of cell plasticity and proliferation modulate posterior regeneration in the annelid Platynereis

  2023cites this paper
• Studying Annelida Regeneration Using Platynereis dumerilii.

  2022cites this paper
• On the hormonal control of posterior regeneration in the annelid Platynereis dumerilii

  2022cites this paper
• Regeneration in the Segmented Annelid Capitella teleta

  2021cites this paper
• Experimental evidence of uncertain future of the keystone ragworm Hediste diversicolor (O.F. Müller, 1776) under climate change conditions.

  2021cites this paper
• Comparative Aspects of Annelid Regeneration: Towards Understanding the Mechanisms of Regeneration

  2021cites this paper
• It Cuts Both Ways: An Annelid Model System for the Study of Regeneration in the Laboratory and in the Classroom

  2021cites this paper
• Neural regulation of body polarities in nereid worm regeneration

  2021cites this paper
• Monsters reveal patterns: bifurcated annelids and their implications for the study of development and evolution

  2021cites this paper
• Regeneration in Annelids: Cell Sources, Tissue Remodeling, and Differential Gene Expression

  2020cites this paper
• Morphallaxis versus Epimorphosis? Cellular and Molecular Aspects of Regeneration and Asexual Reproduction in Annelids

  2020influential citation
• Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii.

  2019cites this paper
• Comparative transcriptomics in Syllidae (Annelida) indicates that posterior regeneration and regular growth are comparable, while anterior regeneration is a distinct process

  2019cites this paper
• The multifaceted role of nerves in animal regeneration.

  2019cites this paper
• A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

  2018cites this paper
• An organizing role for the TGF-β signaling pathway in axes formation of the annelid Capitella teleta.

  2018cites this paper
• Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii

  2018cites this paper
• Regeneration mechanisms in Syllidae (Annelida)

  2018cites this paper
• Regulation of dorso‐ventral polarity by the nerve cord during annelid regeneration: A review of experimental evidence

  2017cites this paper