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The Spiny Mouse, Acomys Cahirinus Malcolm Maden* and Justin A

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The Spiny Mouse, Acomys Cahirinus Malcolm Maden* and Justin A © 2020. Published by The Company of Biologists Ltd | Development (2020) 147, dev167718. doi:10.1242/dev.167718 PRIMER Model systems for regeneration: the spiny mouse, Acomys cahirinus Malcolm Maden* and Justin A. Varholick ABSTRACT Voronstova and Liosner, 1960) and perhaps also chinchillas, cows The spiny mouse, Acomys spp., is a recently described model and pigs (Williams-Boyce and Daniel, 1986). It is also known that organism for regeneration studies. For a mammal, it displays several individual mammalian tissues can regenerate, such as surprising powers of regeneration because it does not fibrose (i.e. skeletal muscle after myotoxin administration (Musarò, 2014) and scar) in response to tissue injury as most other mammals, including the liver, which displays prodigious powers of proliferation during humans, do. In this Primer article, we review these regenerative compensatory hypertrophy (Fausto et al., 2012). This compensatory abilities, highlighting the phylogenetic position of the spiny mouse hypertrophy is a process which the lungs can also undergo (Hsia, relative to other rodents. We also briefly describe the Acomys tissues 2017), whereby the tissue remaining after removal of part of the that have been used for regeneration studies and the common organ expands to compensate for the missing part. Many features of their regeneration compared with the typical mammalian mammalian epithelial tissues, such as the epidermis or the response. Finally, we discuss the contribution that Acomys has made intestinal lining, also exhibit continuous replacement, although in understanding the general principles of regeneration and elaborate this is a property of all animals and so is not considered an unusual hypotheses as to why this mammal is successful at regenerating. regenerative process. Admittedly, all of these regenerative abilities observed in mammals are limited compared with those seen in KEY WORDS: Spiny mouse, Acomys, Tissue regeneration, Fibrosis, axolotls (Joven et al., 2019) or zebrafish (Marques et al., 2019), but Scarring this only represents a very narrow sampling of extant mammalian species and there may be some truly regeneration-competent Introduction mammals out there that remain undiscovered. The field of regenerative medicine aims to identify strategies to Spiny mice, Acomys spp., are one such example of a regeneration- either engineer or repair human tissues, organs and body parts that competent mammal, regenerating several tissues of their body to full cannot naturally be replaced when damaged by trauma or disease. functionality after injury – rather than the reduced functionality Who would not want to take a drug to stimulate the proliferation of normally observed after scarring or fibrosis. Here, we provide an cardiomyocytes and recover from a heart attack? Or, stimulate overview of the history and regenerative abilities of spiny mice. We axonal regrowth across a site of contusion in the spinal cord and propose that if fibrosis can be prevented in humans – as it is in spiny recover function of the lower body and extremities? To solve this mice – then we may be able to regenerate a surprising array of problem of inducing regeneration in humans, conventional wisdom tissues. Moreover, we highlight how the study of spiny mice can suggests that we must identify the molecular and cellular signals that allow us to begin to compare regeneration-competent mammals guide regeneration in regeneration-competent organisms, such as with regeneration-incompetent mammals to discover the cellular axolotls and zebrafish, and extrapolate what we learn to induce it in and molecular signals governing regeneration. regeneration-incompetent organisms such as rats and mice, and eventually humans. General background on Acomys But is it true that mammals really are regeneration-incompetent There are 2050 living species of rodents (which are defined by organisms? The general impression would surely be yes, mammals having upper and lower pairs of continually growing incisors) and cannot regenerate, but a deeper look across the remarkably few two thirds of these belong to the family Muroidea. There are likely species that have been investigated reveals some surprises. For 16 subfamilies of Muroidea including the old world rats (Rattus) example, human children and mice can regenerate their digit tips (Illingworth, 1974; Yu et al., 2019); mammalian fetuses can heal skin wounds in a regenerative manner (Yates et al., 2012); male deer can annually regenerate their antlers, which are initially covered in Model systems for regeneration skin or velvet which itself has regenerated (Goss, 1983); young This article is part of a series entitled ‘Model systems for regeneration’. C57BL/6J mice can regenerate hair follicles via wound-induced hair This series of articles aims to highlight key model systems and species that are currently being used to study tissue and organ regeneration. follicle neogenesis following large skin wounds (Ito et al., 2007); Each article provides background information about the phylogenetic the neonatal mouse heart can regenerate until postnatal day 7 position of the species, its life-cycle and habitat, the different organs and (Porrello et al., 2011); and some species can regenerate large holes tissues that regenerate, and the experimental tools and techniques that punched through their ears, including rabbits (Gawriluk et al., 2016; are available for studying these organisms in a regenerative context. Importantly, these articles also give examples of how the study of these models has increased our understanding of regenerative mechanisms Department of Biology & UF Genetics Institute, University of Florida, PO Box more broadly, and how some of the open questions in the field of 118525, Gainesville, FL 32611, USA. regeneration may be answered using these organisms. To see the full collection as it grows, please visit: https://dev.biologists.org/collection/ *Author for correspondence ([email protected]) regeneration_models. M.M., 0000-0001-7178-5309 DEVELOPMENT 1 PRIMER Development (2020) 147, dev167718. doi:10.1242/dev.167718 11 other subfamilies Acomys cahirinus (Gawriluk et al., 2016; Seifert et al., 2012). All Mus three have been shown to regenerate tissue of the ear following a Muroidea Muridae biopsy punch, although only the regeneration of A. cahirinus has Rattus been studied extensively. Thus, we might assume that regeneration Lophiomys Lophiomyinae is a property of the genus. The colonies that are currently maintained in Europe, USA and Meriones Gerbillinae Australia are A. cahirinus, although one colony of Acomys dimidiatus Deomys is maintained in Geneva (Montandon et al., 2014). Because of their relatively long history of use as laboratory animals, there are several Lophuromys Deomyinae papers published on the care, maintenance and management of Acomys colonies, from early days (Strasser, 1968; Young, 1976) up until the present day (Dickinson and Walker, 2007; Haughton et al., 2016; Uranomys Pinheiro et al., 2018). From these latter works it appears that their Fig. 1. Phylogeny and phenotype of Acomys. Phylogenetic position of the lifespan is usually 3-4 years, but can extend to 6 years. genus Acomys among the 15 sub-families of the family Muridae. There are four Spiny mice have a complex social organization and are often genera including Acomys in the sub-family Deomyinae, the closest relatives of housed in groups of up to 20 to permit communal breeding, which are the gerbils. Adapted from Steppan and Schenk, 2017. although keeping three to five females and one male together in a cage allows the parentage of the pups to be determined (Haughton and mice (Mus), which are placed in the subfamily Muridae et al., 2016). Gestation lasts 39 days, considerably longer than in (Steppan and Schenk, 2017). Spiny mice of the genus Acomys are other rodents, and one to four pups (usually two or three) are placed in one of the other subfamilies called Deomyinae produced. The pups are precocial and born with grey fur, open eyes (previously called Acomyinae) along with Rudd’s mouse and unfurled ears, and they are soon mobile and eating solid food. (Uranomys), the Congo forest mouse or link rat (Deomys), and After 6 weeks, the grey coloured pups (Fig. 2) start producing the the brush-furred mouse (Lophuromys) (Steppan and Schenk, 2017) thick spiny hairs – from posterior to anterior, on the dorsum – and as (Fig. 1). The closest relatives to Deomyinae are the gerbils of the a result change their coat colour to that of the adult (Fig. 2). They subfamily Gerbillinae (Chevret et al., 1993; Steppan and Schenk, become sexually mature at 3-4 months of age (Dieterlen, 1961). 2017) from which they separated 17.6-20 million years ago. Females have an 11-day oestrus cycle after which they undergo There are at least five major groups in the genus Acomys: menstruation (Bellofiore and Evans, 2019). Mating does not result subspinosus, spinosissimus, russatus, wilsoni and cahirinus in the formation of a vaginal plug, making identification of the day (Aghová et al., 2019). All species share morphological of fertilization impossible, although later stages of gestation have characteristics of dorsal spine-like hairs, which are golden brown, been identified by ultrasound (Dickinson and Walker, 2007). grey or rusty brown depending on the species. Ventral hairs are Although spiny mice have recently come to prominence because white. Spiny mice are distributed throughout Africa, the eastern of their striking ability to regenerate several organs and
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