Skin shedding and tissue regeneration in African spiny mice (Acomys)

Abstract

African spiny mice (Acomys) are shown to be capable of regenerating hair follicles, adipose tissue and cartilage, and they can heal deep lesions of skin, with little scarring, suggesting that these mice could prove useful as a model system for studying tissue regeneration in mammals. Many animals can regenerate tissues, organs and even whole limbs after injury. In mammals, this capability is believed to be at best extremely limited, but these authors report that the African spiny mice (Acomys) are potentially important exceptions. Live-trapped A. kempi and A. percivali from Kenya are shown to share with certain lizards the ability to shed and then rapidly regenerate areas of skin. This skin autotomy is an effective defence against predators, who may gain a mouthful of easily-torn skin but miss out on the main prize as the spiny mouse scuttles away. Quite large, deep lesions can be regenerated, complete with hair follicles and cartilage in damaged ears, and with no scarring. The authors propose that these mice produce a pro-regenerative environment similar to that seen in limb-regenerating salamanders. This study suggests that mammals may retain a higher capacity for regeneration than previously recognized, and introduces spiny mice as a novel model organism for study of this subject. Evolutionary modification has produced a spectrum of animal defence traits to escape predation, including the ability to autotomize body parts to elude capture1,2. After autotomy, the missing part is either replaced through regeneration (for example, in urodeles, lizards, arthropods and crustaceans) or permanently lost (such as in mammals). Although most autotomy involves the loss of appendages (legs, chelipeds, antennae or tails, for example), skin autotomy can occur in certain taxa of scincid and gekkonid lizards3. Here we report the first demonstration of skin autotomy in Mammalia (African spiny mice, Acomys). Mechanical testing showed a propensity for skin to tear under very low tension and the absence of a fracture plane. After skin loss, rapid wound contraction was followed by hair follicle regeneration in dorsal skin wounds. Notably, we found that regenerative capacity in Acomys was extended to ear holes, where the mice exhibited complete regeneration of hair follicles, sebaceous glands, dermis and cartilage. Salamanders capable of limb regeneration form a blastema (a mass of lineage-restricted progenitor cells4) after limb loss, and our findings suggest that ear tissue regeneration in Acomys may proceed through the assembly of a similar structure. This study underscores the importance of investigating regenerative phenomena outside of conventional model organisms, and suggests that mammals may retain a higher capacity for regeneration than was previously believed. As re-emergent interest in regenerative medicine seeks to isolate molecular pathways controlling tissue regeneration in mammals, Acomys may prove useful in identifying mechanisms to promote regeneration in lieu of fibrosis and scarring.