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A Marvel of Mammalian Regeneration: Meet the Spiny Mouse


In mammals, where wound healing traditionally culminates in the formation of persistent scars, attention is drawn to a species that defies this age-old norm—a small, unassuming rodent with an extraordinary talent. While stories of legendary regenerative abilities often invoke images of salamanders or starfish, it is time to spotlight this unrecognised member of the animal kingdom. Acomys cahirinus, commonly known as the spiny mouse, has captivated the scientific community with its unparalleled ability to manage wound healing without leaving indelible traces. This captivating mammal might hold the key to unlocking the mystery of scarless and efficient regeneration that could be hiding within the human genome. This article embarks on an expedition to discuss and showcase the intriguing properties of Acomys cahirinus’ healing.


Regeneration in the Animal Kingdom

Regeneration is a natural mechanism by which damaged or absent cells, tissues, organs, and even complete body components are replaced or renewed to restore full functionality (General Medical National Institute of Sciences, n.d.). Regenerative abilities vary among different animals. While numerous metazoan phyla encompass species capable of regenerating lost body parts, the extent of their regenerative aptitude varies significantly (Alvarado, 2000). In invertebrates, creatures like hydra, starfish, annelids, and planarians have well-documented regenerative abilities. Within vertebrates, specific fish and amphibians, including anurans and urodeles, are recognised for their remarkable regenerative capacities (Brockes & Kumar, 2005; Slack et al., 2008). However, in certain groups like birds, nematodes, and cephalochordates, regeneration is rare or mainly absent (Li et al., 2015). Figure 2 illustrates the regenerative prowess of a lizard. A secondary tail can develop either when the original tail is entirely lost, with subsequent lacerations on the stump initiating multiple regenerations, or when the original tail is damaged but not lost, and a new tail grows from the injury site as the original tail simultaneously heals and remains intact.


Figure 1: Model organisms that have great regenerative abilities (Avalos, 2022).

Though it is conventionally believed that mammals generally exhibit limited regenerative responses to injuries, exceptions have intrigued researchers and are a fascinating area of investigation. Epimorphic regeneration is a type of regeneration that involves the regrowth of complex structures from specific stem or progenitor cells, allowing for the replacement of lost or damaged body parts with fully functional tissues or organs (Londono et al., 2018). This remarkable ability to restore lost tissue without causing significant disruptions to the body's structure has led to the development of experimental models such as the 'ear punch' assay. Initially utilised in rabbits, this assay involves creating a circular full-thickness wound in the ear pinna. Notably, the ability to close such ear punches has also been observed in species like cats, pikes, and echolocating bats (Santos et al., 2016).


Understanding regeneration in mammals remains a work in progress, hindered by its infrequent occurrence in this group of animals. Consequently, any reports of new mammals capable of regeneration are of paramount interest. One such report highlighted skin shedding and regeneration in the spiny mouse. These rodents possess a unique trait to shed their fragile, prone to tearing skin, leading to full-thickness wounds that heal rapidly. This regenerative capability extends to their ears, which structurally resemble those of the house mouse. In these spiny mice, full-thickness circular wounds of 4 mm in diameter completely closed in two months, with histological examination revealing the presence of dermis, epidermis, cartilage, hair follicles, and adipose tissue in the regenerated area. Still, muscle tissue was notably absent in the regenerated tissue, and the report did not address the presence of nerve fibres or vasculature (Seifert et al., 2012).


Figure 2: A two-tailed lizard (Wilson, 2019).
Overview of Acomys Cahirinus Species

Acomys cahirinus, known as the spiny mouse, inhabits various arid and semiarid environments in North Africa and the Middle East. This small, nocturnal rodent, weighing just a few tens of grams, might seem unremarkable at first glance. However, its natural habitat and behaviours set it apart (Aghová et al., 2019). These unique creatures can be found in regions characterised by scorching temperatures, limited water sources, and the harsh realities of desert life. To endure these extreme conditions, it has developed efficient water conservation techniques and specialised foraging behaviours tailored to the scarcity of resources. The gestation period is approximately six weeks, which is relatively lengthy for a mouse (21 days in house mice), and the young are well-developed when born (Medger et al., 2010; Whitfield et al., 2018). Extraordinarily, it is the sole documented rodent species to display both spontaneous decidualisation and menstruation (Bellofiore et al., 2017).


Of most importance is the strategy it uses to avoid predation, namely autotomy. Autotomy, or self-amputation, is a term describing the ability of an animal to release the part of the body that a potential predator has caught. In the case of the spiny mouse, the body part in question is its back skin. Remarkably, the process is virtually painless, infection-free, and, most fascinatingly, leads to the complete regeneration of the lost dorsal skin (Jiang et al., 2019). Due to its abilities, the spiny mouse is an extremely appealing model organism for researchers studying regenerative mechanisms.


Figure 3: Acomys cahirinus (Unknown, 2018).
The Process of Skin Regeneration

The initial phase of acute wound healing, known as hemostasis, is a crucial and foundational stage that begins immediately after injury and spans several hours. It is sometimes called the 'lag phase,' during which the organism orchestrates the recruitment of various cells and essential factors for healing despite the absence of mechanical wound strength (Robson et al., 2001). When a skin injury extends beyond the epidermal layer, it means trauma to blood and lymphatic vessels, initiating a flushing process to eliminate microorganisms and antigens from the wound site. This phase activates different clotting cascades, including the extrinsic system driven by clotting factors from the injured skin and the intrinsic system that activates thrombocytes through exposed collagen.


Simultaneously, injured vessels undergo brief vasoconstriction for 5 to 10 minutes, guided by platelets, which control blood loss and create a blood clot rich in cytokines and growth factors (Martin, 1997). This clot also forms the provisional matrix, a structural scaffold for migrating leukocytes, keratinocytes, fibroblasts, and endothelial cells and serves as a container of crucial growth factors for subsequent phases. This vasoconstriction temporarily reduces local perfusion, causing oxygen deprivation, increased glycolysis, and pH changes. Following vasoconstriction, vasodilation occurs, and thrombocytes invade the provisional wound matrix. Platelets release chemotactic factors that influence leukocyte infiltration. Both platelets and leukocytes release cytokines and growth factors, initiating the inflammatory process, stimulating collagen synthesis, triggering the transformation of fibroblasts into myofibroblasts, starting angiogenesis, and supporting early reepithelialisation. The vasodilation phase is characterised by local redness (hyperemia) and wound oedema, indicating ongoing regenerative processes (Eming et al., 2007).


Figure 4: Skin wound healing timeline (Zomer, 2018).

The inflammatory phase in the wound healing process is divided into early and late stages, each marked by the involvement of specific immune cells. Neutrophils, attracted to the injury site by factors like bacterial degradation products, are essential in the initial 2–5 days after injury. They perform phagocytosis, bacterial killing, tissue degradation, and release of inflammatory mediators. These intermediaries enhance the inflammatory response and promote the production of growth factors necessary for proper repair. Neutrophils also release antimicrobial substances and proteinases, contributing to tissue cleaning and renewal. They can also influence macrophages' behaviour, affecting the body's immune response (Daley et al., 2005). Approximately three days after the injury, the late stage of the inflammatory phase commences with the arrival of macrophages at the injury site. Macrophages play a crucial role by phagocytosing pathogens and cellular debris and by secreting various growth factors, chemokines, and cytokines. These substances are instrumental in supporting wound healing and maintaining the overall regenerative process, subsequently activating the phase of cell proliferation and tissue repair (Profyris et al., 2012). Inflammation is crucial for providing signals for cell and tissue movements, which are fundamental for subsequent repair in adult mammals. The level of inflammation may influence the extent of scarring. Besides their immune functions, macrophages play a vital role in effective healing by producing growth factors like TGF-β, TGF-α, basic FGF, PDGF, and VEGF, which stimulate cell growth and the production of extracellular matrix (ECM) components by resident skin cells (Reinke & Sorg, 2012).


During the proliferation phase, occurring approximately 3–10 days post-injury, the primary focus shifts to several critical aspects of the healing process. These include covering the wound's surface, forming granulation tissue, and reestablishing the vascular network. In this phase, local fibroblasts migrate along the fibrin network and initiate reepithelialisation from the wound's edges. Neovascularisation and angiogenesis, involving capillary sprouting, are triggered under the control of regulatory cytokines such as IFN-γ and TGF-β. Fibroblasts play a pivotal role during this stage by synthesising crucial substances like collagen and fibronectin, essential for constructing a new connective tissue matrix. This matrix seals tissue gaps and restores the wound's mechanical strength. Collagen synthesis increases across the wound while fibroblast proliferation gradually diminishes, balancing matrix synthesis and degradation (Reinke & Sorg, 2012).


Figure 5: From cut to cure (Torres, 2023).

Reepithelialisation, the process of renewing the outer epithelial layer, is facilitated by local keratinocytes at the wound's edges and epithelial stem cells from structures like hair follicles or sweat glands. This process activates signalling pathways involving various cytokines and growth factors, including EGF, KGF, IGF-1, and NGF. Moreover, the reduction of contact inhibition and physical tension at cell–to–cell junctions enables lipid mediators and membrane-associated kinases to increase membrane permeability. This change signals the cells at the wound's edges, prompting them to retract and reorganise their internal structures, preparing for migration (Lau et al., 2009). Keratinocytes migrate along a preformed fibrin blood clot in the upper layers of the granulation tissue, a process known as "keratinocyte shuffling" (Jacinto et al., 2001). They move along a chemotactic gradient established by mediators like IL-1 and traverse a fibronectin-rich matrix into the wound's centre. The migration process is characterised by lamellipodial crawling, directed by actin fibre polymerisation and the formation of new focal adhesions at the extracellular matrix mediated by integrins. RhoGTPases (Rho, Rac, Cdc42) regulate these cytoskeletal mechanisms and are vital for coordinating the epithelialisation process and terminating migration (Nobes & Hall, 1999). Migration continues until the cells come into contact with each other, at which point GTPases are likely deactivated, leading to cytoskeleton reorganisation. The fusion of opposing epithelial layers occurs through actin fibre degradation in filopodia, replaced by intercellular adherence contacts, ultimately closing the wound like a zipper (Jacinto et al., 2001).


Restoring the skin's vascular system is a complicated process involving cellular, humoral, and molecular events to reestablish nourishing blood flow. Growth factors like VEGF, PDGF, bFGF, and thrombin are initiators. These growth factors bind to receptors on existing endothelial cells, activating intracellular signalling cascades. Those connections prompt endothelial cells to secrete proteolytic enzymes, dissolving the basal lamina and allowing them to proliferate and migrate, a process known as "sprouting". Endothelial cells rely on adhesion molecules like integrins (αvβ3, αvβ5, α5β1) and release matrix metalloproteinases to facilitate tissue lysis during proliferation. The sprouts form small tubular canals that interconnect, eventually differentiating into arteries and venules and stabilising their walls with pericytes and smooth muscle cells. The newly formed vessels complete the angiogenic process. In full–thickness dermal wounds, vascularisation follows a distinct pattern, with an inner ring of circular vessels initially forming at the wound margin, followed by outer radially arranged vessels supplying the inner ones. As wound closure progresses, the inner vascular ring shrinks while the radially arranged vessels interconnect, forming a new dermal vascular network (Reinke & Sorg, 2012).


Figure 6: Wound healing in humans results in scar formation (Unknown, 2023).

The final step in the proliferation phase is the development of acute granulation tissue. This transitional tissue replaces the provisional wound matrix and contains a high density of fibroblasts, granulocytes, macrophages, capillaries, and loosely organised collagen bundles. The fibroblast is the predominant cell in this phase and is crucial in producing collagen and ECM substances. ECM provides a scaffold for cell adhesion and regulates cell growth, movement, and differentiation. At the end of this phase, myofibroblast differentiation reduces the number of maturing fibroblasts.


The remodelling phase, occurring from day 21 to up to 1 year after injury, involves apoptosis of the cells, resulting in a mature, avascular, and acellular wound. During wound maturation, collagen III is replaced by stronger collagen I, and myofibroblasts contribute to wound contractions by attaching to collagen. Angiogenesis diminishes, wound blood flow decreases, and metabolic activity slows down and eventually ceases (Nguyen & Soulika, 2019).


The Regenerative Ability of the Spiny Mouse

As previously mentioned, the spiny mouse exhibits an impressive capacity for skin regeneration, capable of fully restoring hair follicles, sebaceous glands, and dermal tissue following skin injuries caused by self-defence autotomy without leaving any trace. Remarkably, the regenerative prowess of this unique rodent also extends to its internal organs. The fact that a mammal displays such regenerative mastery has reignited enthusiasm and renewed hope that efficient, scarless healing may be attainable for humans. Consequently, the spiny mouse has become an invaluable model for studying regeneration. In research settings, wound healing processes in the spiny mouse are often compared to those in house mice (Mus). Studies examining gene expression profiles during skin regeneration have revealed significant differences in the extracellular matrix composition. Mus wounds exhibit elevated levels of TIMP1 and low expression of Fn1, MMP9, and MMP13, resulting in a high collagen I to III ratio. In contrast, wounds of the spiny mouse display high levels of Fn1, MMP9, and MMP13, along with a high collagen III to I ratio (Gawriluk et al., 2016). Furthermore, immune responses between the two species differ, with Mus showing more elevated interleukin and chemokine expression. Notably, the spiny mouse regenerates all three hair types shortly after injury, and it closes wounds rapidly with a reduced presence of myofibroblasts, contrary to Mus (Brant et al., 2016).


Figure 7: Summary of the organs and tissues in the spiny mouse that have been investigated for regenerative ability (Sandoval, 2020).

Adult spiny mice demonstrate an unprecedented ability to restore cardiac function and myocardial structure following coronary artery ligation, a condition typically associated with significant heart damage. This exceptional cardiac recovery makes it the first adult mammal to display such regenerative capabilities in the myocardium. The spiny mouse has previously shown regenerative potential in various tissue types, including dermal components, hair, kidneys, and skeletal muscle, all healing without scarring after injury (Maden et al., 2018; Okamura et al., 2018). The absence of fibrotic responses in these regenerative processes led researchers to hypothesise that this model organism may have evolved mechanisms to prevent fibrosis following damage. To investigate whether this hypothesis holds not only for skin wounds but also for internal organ damage, Qi and colleagues conducted coronary artery ligation to induce myocardial infarction in adult spiny mice. The research revealed that they could indeed recover myocardial function even after this life-threatening cardiac injury, shedding light on the cardioprotective and regenerative signalling mechanisms unique to this species (Qi et al., 2021).


Seifert and colleagues analysed the mechanical properties of the spiny mouse's skin, which is remarkably weak and prone to tearing. It exhibited brittleness, fracturing shortly after load application, in contrast to Mus' skin, which displayed elasticity and was approximately 20 times stronger. Despite its fragile skin, the spiny mouse displayed rapid and scar-free wound healing, with exceptional re-epithelialisation, relying heavily on wound edge contraction. The model organism's wound extracellular matrix exhibited unique characteristics favouring regeneration over scarring, featuring a more porous structure and a prevalence of collagen type III over collagen type I. This outcome aligns with the findings of other researchers. The spiny mouse also demonstrated the regeneration of hair follicles, driven by a highly proliferative population of epidermal cells expressing keratin-17. In contrast, house mice could not regenerate hair follicles following similar injuries, indicating a deficiency in the underlying dermal signals required for regeneration. Proliferation was widespread in both the spiny and the house mouse's wounds, but key differences were observed, especially in the distal epidermis (Seifert et al., 2012).


Figure 8: The spiny mouse—an emerging model in regenerative medicine (Okamura, 2022).

Yoon et al. also compared skin regeneration in the spiny mouse with skin scarring in house mice after similar injuries. The study revealed striking similarities between the former and fetal wound healing, such as the absence or low levels of pro-inflammatory cytokines, reduced F4/80 macrophages, and distinct extracellular matrix components (Yoon et al., 2020). Unlike Mus, which demonstrated excessive collagen production, the spiny mouse did not exhibit this characteristic (Brant et al., 2015). Macrophages play a crucial role in regeneration, even though they may not always be present at the wound site (Simkin et al., 2017). Nevertheless, an acute inflammatory response was observed in both animals, with more vigorous reactive oxygen species production in the spiny mouse. The study offered insights into the differences between these species at the cellular and genetic levels. Qualitative and quantitative comparisons of proteomic profiles revealed distinctions in ubiquitin-related enzymes, phosphorylation-associated proteins, proteases, immunomodulators, and macrophage markers. Yoon's study highlights the significance of enhanced protein degradation and synthesis in the spiny mouse, mainly through ubiquitination and phosphorylation, which likely regulate signalling pathways crucial for tissue repair. Additionally, the varying macrophage profiles may lead to different extracellular matrix microenvironments, influencing the healing outcome, with fibrosis in Mus and regenerative response in the spiny mouse (Yoon et al., 2020).


Conclusions

The regenerative capabilities of the spiny mouse are fascinating. It displays a unique ability to fully restore skin, including hair follicles, sebaceous glands, and dermal tissue, following injuries induced by self-defence autotomy. These regenerative processes make Acomys cahirinus a valuable model for studying the complex regeneration of specialised structures within the skin and other tissues. Comparative studies with Mus have unveiled significant differences in gene expression, extracellular matrix composition, immune responses, and hair follicle regeneration, emphasising the distinct regenerative mechanisms at play. While human skin possesses a degree of regenerative capacity, the realisation of complete scarless healing, as exemplified in the spiny mouse, has long been an aspiration in regenerative medicine. Pursuing this objective hinges on unravelling the molecular and genetic underpinnings of regeneration within unique models, such as the spiny mouse, which offers promising prospects for innovative therapies aimed at augmenting wound healing and diminishing scar formation in humans both externally and internally.


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Convidado:
12 de nov. de 2023
The spiny mouse is a phenomenal creation of nature. This is a mammal capable of amazing acts of regeneration, standing out among other species for its ability to restore tissues and organs. I wrote a dissertation about this species dissertation writer for hire here they helped me to complete my assignment perfectly without errors.
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