Literature DB >> 19966282

Latent regeneration abilities persist following recent evolutionary loss in asexual annelids.

Alexandra E Bely1, James M Sikes.   

Abstract

Regeneration abilities have been repeatedly lost in many animal phyla. However, because regeneration research has focused almost exclusively on highly regenerative taxa or on comparisons between regenerating and nonregenerating taxa that are deeply diverged, virtually nothing is known about how regeneration loss occurs. Here, we show that, following a recent evolutionary loss of regeneration, regenerative abilities can remain latent and still be elicited. Using comparative regeneration experiments and a molecular phylogeny, we show that ancestral head regeneration abilities have been lost three times among naidine annelids, a group of small aquatic worms that typically reproduce asexually by fission. In all three lineages incapable of head regeneration, worms consistently seal the wound but fail to progress to the first stage of tissue replacement. However, despite this coarse-level convergence in regeneration loss, further investigation of two of these lineages reveals marked differences in how much of the regeneration machinery has been abolished. Most notably, in a species representing one of these two lineages, but not in a representative of the other, amputation within a narrow proliferative region that forms during fission can still elicit regeneration of an essentially normal head. Thus, the presence at the wound site of elements characteristic of actively growing tissues, such as activated stem cells or growth factors, may permit blocks to regeneration to be circumvented, allowing latent regeneration abilities to be manifested.

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Year:  2009        PMID: 19966282      PMCID: PMC2824374          DOI: 10.1073/pnas.0907931107

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  19 in total

1.  Neoblasts and limitation of the cephalic regenerative capacity of the planarian Dendrocoelum lacteum

Authors:  S KOLMAYER; F STEPHAN-DUBOIS
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2.  Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I.

Authors:  Alexandra E Bely; Gregory A Wray
Journal:  Mol Phylogenet Evol       Date:  2004-01       Impact factor: 4.286

3.  Molecular evidence for the non-monophyletic status of Naidinae (Annelida, Clitellata, Tubificidae).

Authors:  Ida Envall; Mari Källersjö; Christer Erséus
Journal:  Mol Phylogenet Evol       Date:  2006-05-08       Impact factor: 4.286

4.  Evolutionary modification of regenerative capability in vertebrates: a comparative study on teleost pectoral fin regeneration.

Authors:  G P Wagner; B Y Misof
Journal:  J Exp Zool       Date:  1992-01-01

Review 5.  Bridging the regeneration gap: genetic insights from diverse animal models.

Authors:  Alejandro Sánchez Alvarado; Panagiotis A Tsonis
Journal:  Nat Rev Genet       Date:  2006-11       Impact factor: 53.242

6.  Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii.

Authors:  N Rebscher; F Zelada-González; T U Banisch; F Raible; D Arendt
Journal:  Dev Biol       Date:  2007-04-01       Impact factor: 3.582

Review 7.  Comparative aspects of animal regeneration.

Authors:  Jeremy P Brockes; Anoop Kumar
Journal:  Annu Rev Cell Dev Biol       Date:  2008       Impact factor: 13.827

8.  Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (Gymnophthalmidae: Squamata).

Authors:  Tiana Kohlsdorf; Günter P Wagner
Journal:  Evolution       Date:  2006-09       Impact factor: 3.694

9.  Suppression of the immune response potentiates tadpole tail regeneration during the refractory period.

Authors:  Taro Fukazawa; Yuko Naora; Takekazu Kunieda; Takeo Kubo
Journal:  Development       Date:  2009-06-10       Impact factor: 6.868

10.  Evolution of regeneration and fission in annelids: insights from engrailed- and orthodenticle-class gene expression.

Authors:  A E Bely; G A Wray
Journal:  Development       Date:  2001-07       Impact factor: 6.868

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  17 in total

Review 1.  Indeterminate Growth: Could It Represent the Ancestral Condition?

Authors:  Iswar K Hariharan; David B Wake; Marvalee H Wake
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-07-27       Impact factor: 10.005

2.  A phylum-wide survey reveals multiple independent gains of head regeneration in Nemertea.

Authors:  Eduardo E Zattara; Fernando A Fernández-Álvarez; Terra C Hiebert; Alexandra E Bely; Jon L Norenburg
Journal:  Proc Biol Sci       Date:  2019-03-13       Impact factor: 5.349

3.  Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle.

Authors:  Bertanne Visser; Cécile Le Lann; Frank J den Blanken; Jeffrey A Harvey; Jacques J M van Alphen; Jacintha Ellers
Journal:  Proc Natl Acad Sci U S A       Date:  2010-04-26       Impact factor: 11.205

4.  Wound healing and blastema formation in regenerating digit tips of adult mice.

Authors:  Warnakulasuriya Akash Fernando; Eric Leininger; Jennifer Simkin; Ni Li; Carrie A Malcom; Shyam Sathyamoorthi; Manjong Han; Ken Muneoka
Journal:  Dev Biol       Date:  2010-12-08       Impact factor: 3.582

5.  The giant danio (D. aequipinnatus) as a model of cardiac remodeling and regeneration.

Authors:  Pascal J Lafontant; Alan R Burns; Jamie A Grivas; Mary A Lesch; Tanmoy D Lala; Sean P Reuter; Loren J Field; Tyler D Frounfelter
Journal:  Anat Rec (Hoboken)       Date:  2011-11-18       Impact factor: 2.064

6.  Studying Annelida Regeneration in a Novel Model Organism: The Freshwater Aeolosoma viride.

Authors:  Chiao-Ping Chen; Sheridan Ke-Wing Fok; Cheng-Yi Chen; Fei-Man Hsu; Yu-Wen Hsieh; Jiun-Hong Chen
Journal:  Methods Mol Biol       Date:  2022

Review 7.  Mammalian organ regeneration in spiny mice.

Authors:  Daryl M Okamura; Elizabeth D Nguyen; Sarah J Collins; Kevin Yoon; Joshua B Gere; Mary C M Weiser-Evans; David R Beier; Mark W Majesky
Journal:  J Muscle Res Cell Motil       Date:  2022-09-21       Impact factor: 3.352

8.  Transcriptome characterization via 454 pyrosequencing of the annelid Pristina leidyi, an emerging model for studying the evolution of regeneration.

Authors:  Kevin G Nyberg; Matthew A Conte; Jamie L Kostyun; Alison Forde; Alexandra E Bely
Journal:  BMC Genomics       Date:  2012-06-29       Impact factor: 3.969

9.  A pan-metazoan concept for adult stem cells: the wobbling Penrose landscape.

Authors:  Baruch Rinkevich; Loriano Ballarin; Pedro Martinez; Ildiko Somorjai; Oshrat Ben-Hamo; Ilya Borisenko; Eugene Berezikov; Alexander Ereskovsky; Eve Gazave; Denis Khnykin; Lucia Manni; Olga Petukhova; Amalia Rosner; Eric Röttinger; Antonietta Spagnuolo; Michela Sugni; Stefano Tiozzo; Bert Hobmayer
Journal:  Biol Rev Camb Philos Soc       Date:  2021-10-06

10.  Fine taxonomic sampling of nervous systems within Naididae (Annelida: Clitellata) reveals evolutionary lability and revised homologies of annelid neural components.

Authors:  Eduardo E Zattara; Alexandra E Bely
Journal:  Front Zool       Date:  2015-04-18       Impact factor: 3.172

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