Closing the wounds: One hundred and twenty five years of regenerative biology in the ascidian Ciona intestinalis

Abstract

This year marks the 125th anniversary of the beginning of regeneration research in the ascidian Ciona intestinalis. A brief note was published in 1891 reporting the regeneration of the Ciona neural complex and siphons. This launched an active period of Ciona regeneration research culminating in the demonstration of partial body regeneration: the ability of proximal body parts to regenerate distal ones, but not vice versa. In a process resembling regeneration, wounds in the siphon tube were discovered to result in the formation of an ectopic siphon. Ciona regeneration research then lapsed into a period of relative inactivity following the purported demonstration of the inheritance of acquired characters using siphon regeneration as a model. Around the turn of the present century, Ciona regeneration research experienced a new blossoming. The current studies established the morphological and physiological integrity of the regeneration process and its resemblance to ontogeny. They also determined some of the cell types responsible for tissue and organ replacement and their sources in the body. Finally, they showed that regenerative capacity is reduced with age. Many other aspects of regeneration now can be studied at the mechanistic level because of the extensive molecular tools available in Ciona.

Reconsidering regeneration in metazoans: an evo-devo approach

“…Colonial ascidians seem to employ totipotent stem cells, expressing Piwi and Vasa markers, during whole body regeneration in botrillidae (Brown et al, 2009a), but in other species cell transdifferentiation is implicated (Kawamura et al, 2013), or even the coexistence of multiple systems, involving the presence and dedifferentiation of multipotent epithelial cells and mobile cells (Kawamura et al, 2008;Tiozzo et al, 2008). In Ciona intestinalis, a solitary species of ascidian, the regeneration of the oral siphon involves the local differentiation of progenitor cells whose identity is uncertain (Auger et al, 2010;Jeffery, 2015). In vertebrates the modus operandi of the regenerative precursor differs.…”

“…The literature on this topic has been enriched with new laboratory models thanks to adaptable technical protocols and more affordable access to genomic and transcriptomic approaches (Vickery et al, 2001;Candia Carnevali, 2006;Kürn et al, 2011;Bely, 2014;Jeffery, 2015). Knowledge of more classical models such as planarians, annelids, and urodela has grown, providing important findings on the cellular and molecular dynamics of their regeneration potentials (Alvarado and Tsonis, 2006;Tanaka and Reddien, 2011;Bely, 2014).…”

A microRNA-mRNA expression network during oral siphon regeneration in Ciona

“…The colonial tunicates, such as Botryllus schlosseri, show whole-body regeneration (Kürn et al, 2011;Rinkevich et al, 1995Rinkevich et al, , 2010Voskoboynik et al, 2007). Ciona intestinalis and Ciona robusta, two species that until recently were both called Ciona intestinalis (Brunetti et al, 2015), are well-established models for embryology, and as adults they can rapidly and robustly regenerate their oral siphons as well as their central nervous systems (Jeffery, 2015a). The oral siphon (OS) is a cylindrical appendage composed primarily of muscular tissue, vasculature, nerves, epidermis, eight oral pigment organs (OPOs) located at the distal tip, and an outer coating of tunic (Chiba et al, 2004).…”

Regeneration, Stem Cells, and Aging in the Tunicate Ciona

“…1A, B). The newly formed distal body tissues and organs first become capable of regeneration after metamorphosis (Jeffery, 2015b). The mechanisms responsible for the conversion of a non-regenerating larva into a regenerating adult are unknown in Ciona and other tunicates.…”

“…The phenomenon of distal regeneration from proximal parts of the adult body was termed "partial body regeneration" (Jeffery, 2015b) to distinguish it from other types of regeneration displayed by ascidians: bipolar regeneration in Clavellina (Brien, 1968) and whole body regeneration in colonial ascidians (Freeman, 1964;Tiozzo et al, 2008;Brown and Swalla, 2012).…”