Considering the evolution of regeneration in the central nervous system

Abstract

For many years the mammalian CNS has been seen as an organ that is unable to regenerate. However, it was also long known that lower vertebrate species are capable of impressive regeneration of CNS structures. How did this situation arise through evolution? Increasing cellular and molecular understanding of regeneration in different animal species coupled with studies of adult neurogenesis in mammals is providing a basis for addressing this question. Here we compare CNS regeneration among vertebrates and speculate on how this ability may have emerged or been restricted.

The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration

“…Also in Hydra the recent possibility to establish transgenic strains allows investigators to follow live the cellular remodeling that takes place Box 1: Phylogenetic tree showing the animal phyla that contain species with high regenerative potential. All species schematized here provide useful model systems to study the biology of adult stem cells and the mechanisms supporting adult regeneration 1,2,31,57,70 . By contrast Caudata (Xenopus) and Insects (Drosophila, cricket) only regenerate their appendages at the larval stage but provide valuable model systems to test the impact of extinguishing developmental processes on regenerative programs 73 and to dissect the genetic pathways involved in apoptosis-induced compensatory proliferation [58][59][60] .…”

“…Although the capacity to undergo regeneration is widespread among members of the animal kingdom, whether there is a core sequence of cellular processes that similarly drives regeneration in evolutionarily distant regenerative contexts remains an open question 1,2,31,57 . Recently, the apoptosisinduced compensatory proliferation was proposed to provide a conserved mechanism to trigger regeneration in contexts as different as the Drosophila larva regenerating its imaginal discs after cell death induction [58][59][60] , the Xenopus tadpole regenerating its tail after amputation 61 , the Hydra polyp regenerating its head after mid-gastric bisection 39 , or the mouse repairing its skin after damage and liver after partial hepatectomy 62 .…”

Vertebrate-like regeneration in the invertebrate chordate amphioxus

“…A question of general interest is why certain lineages have lost or reduced regenerative capacity relative to their regeneration-competent sister taxa. In particular, the properties of CNS regeneration in more basal vertebrates may shed light on the reasons for reduced capacity in mammals and birds (2). Despite the plethora of hypotheses that attempt to explain the evolutionary significance of regenerative ability, the unresolved central issue is whether the ability to regenerate is adaptive or simply a byproduct of selection on other metabolic or developmental processes.…”

Entre homéostasie et développement, quelles stratégies pour régénérer ?

“…Tandis que la réparation tissulaire et la régénération sont induites par des forces externes (blessure, lésions tissulaires, amputation), le renouvellement tissulaire qui résulte de la combinaison de la prolifération, de la mort et de la différenciation cellulaires, répond plus généralement à des signaux endogènes (Pellettieri & Sanchez Alvarado, 2007). (Tanaka and Ferretti, 2009;Galliot and Ghila, 2010).…”

“…Le modèle de l'Hydre confirme le lien entre prolifération compensatrice induite par l'apoptose et régénération Bien que la régénération soit largement distribuée au sein du royaume animal, la question de savoir si des mécanismes de base sont partagés par différentes espèces au cours de cette régénération est loin d'être résolue (Brockes & Kumar, 2008;Tanaka & Ferretti, 2009;Bely & Nyberg, 2010). Récemment, nous avons proposé que la prolifération compensatrice induite par l'apoptose agisse comme un mécanisme conservé capable de déclencher une réponse de type régénératif à une blessure.…”