Amphioxus regeneration: evolutionary and biomedical implications

Abstract

Regeneration is a variable trait in chordates, with some species capable of impressive abilities, and others of only wound healing with scarring. Regenerative capacity has been reported in the literature for 5 species from two cephalochordate genera, Branchiostoma and Asymmetron. Its cellular and molecular bases have been studied in some detail in only two species: tail regeneration in the European amphioxus B. lanceolatum; and oral cirrus regeneration in the Asian species B. japonicum. Gene expression analyses of germline formation and posterior elongation in cephalochordate embryos provide some insight into regulation of progenitor and stem cell function. When combined with functional studies of gene function, including overexpression and knockdown, these will open the door to amphioxus as a good model not only for understanding the evolution of regeneration, but also for biomedical purposes.

Tail regeneration in a cephalochordate, the Bahamas lancelet,Asymmetron lucayanum

“…The more recent studies of cephalochordate tail regeneration have concerned Branchiostoma lanceolatum cultured at 19°C (Somorjai, 2017; Somorjai et al, 2012) and B. japonicum (Liang et al, 2019) cultured at an unreported temperature. For both, the rate of tail regrowth was considerably slower than in A. lucayanum maintained at 28 ° C. For example, the regeneration stage reached in 4 days in A. lucayanum was equivalent to that reached in 14 days and 25 days, respectively, in B. lanceolatum and B. japonicum .…”

“…There are three genera of cephalochordates (Nishikawa, 2018). Their regeneration is best known for Branchiostoma (Bieberhofer, 1906; Bone & Azariah, 1992; Kaneto & Wada, 2011; Liang, Rathnayake, Huyang, Pathirana, & Zhang, 2019; Pegeta, 1992; Probst, 1930; Silva, Mendes, & Mariano, 1995; Somorjai, 2017; Somorjai, Somorjai, Garcia‐Fernàndez, & Escrivà, 2012), with only a single study being devoted to Asymmetron (Andrews, 1893) and none to Epigonichthys . This taxonomically lop‐sided coverage is unfortunate because details about regeneration can sometimes differ between close relatives.…”

BMP signaling is required for amphioxus tail regeneration

“…Thus, it is an ideal animal in which to investigate the evolution of regenerative ability and mechanisms in chordates from the invertebrate to vertebrate transition. In fact, amphioxus has long been used to study regeneration, and the history of studies on regeneration of amphioxus has been recently reviewed (Somorjai, 2017). It was initially reported to possess a generally poor potential to replace lost body parts (Biberhofer, 1906;Probst, 1930) but was later shown to have a remarkably high capacity to regenerate tail and oral cirri after amputation (Somorjai et al, 2012a;Kaneto and Wada, 2011;Silva et al, 1998).…”

Appendage regeneration in anamniotes utilizes genes active during larval‐metamorphic stages that have been lost or altered in amniotes: The case for studying lizard tail regeneration

“…It is here considered that organ regeneration in piscine vertebrates is an ancestral process that derives from the restructuring and regenerative processes present in their invertebrate chordate ancestors, as supported from the observation of the broad regenerative ability still present in extant cephalochordates such as Branchiostoma (Somorjai, 2017). The ability to regenerate various organs in different vertebrates derives from their specific evolutionary history: this consideration represents the guiding theme of the present manuscript that aims to explain the biological reasons why only few vertebrates can broadly regenerate organs.…”