Use of induced pluripotent stem cells for regenerative medicine and understanding of cell biology
Kaiana Recchia A B , Laís Vicari de Figueiredo Pessôa B , Naira Caroline Godoy Pieri B and Fabiana Fernandes Bressan A B *A
B
Abstract
Stem cells are a highly desirable tool for regenerative medicine due to unique characteristics such as immunomodulation and angiogenesis (multipotent cells) and high self-renewal potential and differentiation capability (pluripotent cells), thus being classified according to their stage of dedifferentiation and epigenetic profile. Apart from being used for in vitro disease modeling or even in vivo therapies, pluripotent stem cells are a valuable tool for animal production and breeding improvement. In particular, due to the lack of robustness and ethical concerns regarding embryonic stem cells, induced pluripotent stem cells (iPSCs) emerge as a new ‘game changer’ in veterinary and translational medicine. Herein, we present and discuss recent potential uses of stem cells in medicine and understanding cell biology, focusing on generating and using iPSCs from diverse species aiming for genetic conservation or dissemination using in vitro gametogenesis, cellular therapies, and cellular agriculture.
Keywords: cellular agriculture, genetic improvement, in vitro gametogenesis, iPSCs, PGCLCs, pluripotent stem cells, regenerative medicine, stem cells.
Introduction
Stem cells are undifferentiated, self-renewing cells that present new possibilities for regenerative medicine and understanding early mammalian development. Adult multipotent stem cells are already widely used worldwide in human and veterinary medicine, and their therapeutic signaling, especially regarding immunomodulation and trophic properties, has been intensely studied and reported. In contrast, the derivation of pluripotent embryonic stem cells (ESCs) is more profoundly studied and reported in human and mice models only. Indeed, a clear elucidation of the molecular pathways involved in pluripotency acquisition has been recently reported (Ishiuchi and Torres-Padilla 2013; Yeh et al. 2021; Ishiuchi and Sakamoto 2023). For example, Du and Wu (2024) have elegantly discussed and proposed molecular and functional hallmarks to adequately define pluripotency and totipotent states in mice and humans. In contrast, the derivation and maintenance of ESCs in domestic species, despite recent milestones achieved regarding expanded and primed swine and cattle pluripotent cells (Bogliotti et al. 2018; Gao et al. 2019; Zhao et al. 2021), is still challenging and needs further studies from other research groups before reaching a robust worldwide protocol for maintenance of in vitro pluripotency (Brevini et al. 2008; Gandolfi et al. 2012; Nowak-Imialek and Niemann 2013; Pieri et al. 2019).
More recently, the generation of induced pluripotent stem cells (iPSCs) through forced expression of specific transcription factors has been demonstrated in domestic and wild species, and has endowed new possibilities in regenerative medicine and reproductive science based on the ability of these cells to differentiate into a variety of cell types in vitro. The development of iPSCs from animals enabled researchers to overcome the barriers related to working with ESCs, making possible the development of autologous therapies without the use of embryos, for example.
The acquisition of iPSCs has been reported in different species such as humans, mice, domestic (pets and farm animals) and wild animals (Takahashi and Yamanaka 2006; Takahashi et al. 2007; Zhou et al. 2011; Guo et al. 2018; Qi et al. 2018; Bressan et al. 2020; Machado et al. 2020; Bessi et al. 2021; de Souza et al. 2021; Botigelli et al. 2022; Recchia et al. 2022), reviewed by Pessôa et al. (2019a). Using iPSCs from domestic or wild species may contribute significantly to reproductive technologies, offering unprecedented opportunities to restore fertility, preserve endangered species, and generate transgenic animals for biomedical applications. For example, iPSCs have been differentiated into primordial germ cells (PGC-like cells, PGCLs) and functional gametes in mice (Hayashi et al. 2011, 2012).
Once pluripotent stem cells (PSCs) such as ESCs or iPSCs have the plasticity to differentiate into the three germ layers (mesoderm, endoderm, or ectoderm), such cells also emerge as an option to develop other cutting-edge biotechnologies. Examples of such are the derivation of ‘cell chips’ aiming to mimic biological processes in vitro, embryoids, or even cell-cultured meat, as they can be differentiated into all the cell types and functional tissues (Fig. 1) (Świerczek et al. 2015; Chal and Pourquié 2017; Fan et al. 2021; Leung et al. 2022).
Somatic cells may be in vitro reprogrammed to acquire pluripotency. This process is of significant importance as it leads to the generation of induced pluripotent cells from domestic and wild animals. These cells have the potential to profoundly contribute to regenerative and translational medicine, such as generating functional cells and tissues for in vivo or in vitro applications. They may also contribute to the field of cellular agriculture by contributing to the generation of specific tissues in a large-scale manner.
Therefore, this review discusses, in particular, studies on the steps necessary for cell reprogramming to generate functional tissues for regenerative medicine or cellular agriculture. It also aims to contribute to the generation of genetically superior or modified individuals for agricultural or biomedical applications through in vitro gametogenesis.
Acquisition of toti or pluripotency in animal models: cellular reprogramming
A fundamental question of science throughout time is pursuing a precise non-stochastic understanding of the mechanisms by which a cell decides its fate, that is, its shape, function, and positioning, during the organism’s development. The cell is the basic unit of life and heredity, and can assume different phenotypes after intrinsic and extrinsic stimuli or genetic and epigenetic, respectively. The need for precise molecular events that lead to countless possibilities of cellular fates is evident, which are continuous and finely regulated, from totipotency to the formation of specialized tissues, including the correct dissemination of genetic material, and, therefore, guaranteeing the transmission of genetic material between generations.
In this sense, cell reprogramming is undoubtedly one of the most promising tools in current science. Modulating cell and tissue phenotype to the form and function of interest opens the possibility of creating entirely new ways to manipulate the characteristics of plants and animals, enabling the creation of advantages in all areas of science and promoting new technologies and concepts in medical and agricultural sciences.
The acquisition of pluripotency through reprogramming, or at least a state similar to embryonic pluripotency, has been reported in several species in recent years, and herein we cite some of the results in large animals accomplished by our research group (Pessôa et al. 2019b; Bressan et al. 2020; de Castro et al. 2020; Machado et al. 2020; Bessi et al. 2021; Pieri et al. 2022). Therefore, molecular mechanisms are considered somewhat conserved, although notable differences exist between species. However, generating bonafide iPSCs in such species has been challenging since the iPSC technology breakthrough in mouse and humans. Our group has reviewed, as well as many others, that the same protocols and pluripotency profiles of mouse/human iPSCs do not apply to other animals equally (Pessôa et al. 2019a).
Significant advances have been made in understanding pluripotency acquisition during reprogramming, considered a highly heterogeneous process (Hayashi et al. 2019). For example, the mesenchymal-to-epithelial transition has long been reported as an essential step for pluripotency acquisition (Li et al. 2010). More recently, Guo et al. (2019) demonstrated two other relevant pathways essential to determining the reprogrammed fate through mouse reprogramming. Using the single-cell resolution analysis, they showed that the Klf4 transcription factor contributes to the non-reprogrammed Cd34+/Fxyd5+/Psca+ keratinocyte-like fate and that IFN-γ impedes the final transition to chimera-competent pluripotency along with the reprogrammed cells (Guo et al. 2019). Nonetheless, a detailed description of a time-lapse gene expression analysis during reprogramming and pluripotency maintenance in other species (rather than human/mouse) is still absent in the literature.
The consolidation of the generation and use of induced pluripotent stem cells (or iPSCs) in different species has the great advantage of generating cells with pluripotent characteristics, which can be genetically edited, and are able, through germline induction, to derive totipotent cells, leading to the generation of offspring, with known genetics, and also creating an ideal platform for in vitro and in vivo modeling of several syndromes (Cherry and Daley 2013; Nakamura et al. 2013; Peitz et al. 2013; Arai et al. 2015; Saito 2018).
iPSCs for translational and regenerative medicine
Animal models have long been valuable in science, and most recently, in vitro animal models have proven to be more accessible and sometimes less expensive to maintain while just as valuable tools, with particular remark for pluripotent stem cells. Although embryonic stem cells were isolated first (Evans and Kaufman 1981; Martin 1981), throughout the last years and since iPSCs were generated, they have gained more attention due to their plasticity and their ‘embryo-free’ nature, in addition to the shared characteristics with ESC (Takahashi and Yamanaka 2006; Takahashi et al. 2007), and more recently, the possibility of gene editing. Considering animal models, iPSCs have been generated from a wide variety of species, including companion, farm, and wild animals, as described before. The derivation of pluripotent stem cells in vitro for each species is consequent to the different expected outreaches, such as the generation of bioreactors and the in vitro production of animal-derived products such as leather and meat from farm species, the preservation of endangered species by deriving gametes or embryos in vitro, besides the possible uses in regenerative medicine and the creation of disease models from diverse species (Cong et al. 2019; Pieri et al. 2019).
Regarding companion animals, canines are remarkable models, presenting a couple of hundred naturally occurring diseases similar to humans and other anatomical and physiological similarities (Hyttel et al. 2019). For instance, canine iPSCs have been used to develop therapeutic approaches for canine cognitive dysfunction, a condition similar to Alzheimer’s (Chandrasekaran et al. 2021). Also, canine iPSC-derived neural progenitor cells have been used in a pilot study as an attempt to treat chronic spinal cord injury. Although no clinical improvement was detected in the animals, tumors were also not detected in follow-up appointments (Chow et al. 2020), highlighting the importance of the model in pre-clinical studies.
Considering farm animals, multiple studies have approached equine iPSCs and their value for regenerative medicine and as models for skeletal muscle affections (Pessôa et al. 2019b; de Castro et al. 2020). Bovine iPSCs have also gathered attention, mainly when reflecting on new sources for animal-derived products and reproduction. Studies regarding porcine iPSCs are a majority, and due to the shared characteristics with humans, porcine are the go-to translational model, especially for heart dysfunctions (Hyttel et al. 2019; Sridharan et al. 2023). Porcine iPSCs have been differentiated into various cells, such as neural progenitor cells and primordial germ cells (Machado et al. 2020; Pieri et al. 2022). From the clinical perspective, iPSCs associated with biodegradable scaffolds have been used to treat retinal degradation in pigs (Sharma et al. 2019). In miniature pigs, iPSC-derived osteoblast-like cells and neuronal progenitor cells were used to treat porcine bone loss and Parkinson’s disease artificial models, respectively. Interestingly, improvement post-cell transplantation was detected in both cases (Liao et al. 2018, 2023). Indeed, the porcine is probably the most studied ‘non-human and non-mouse’ species due to its physiological and morphological similarity to humans, turning it into an attractive biomedical model.
In regard of wild animals, iPSCs generated are a remarkable asset for species preservation, especially with the methodologies for in vitro gamete production, as discussed below. However, considering the therapeutic perspective, the most relevant iPSC-based model must be non-human primates. There are over a hundred studies on the isolation and characterization of non-human primates’ pluripotent stem cells, including iPSCs, using different cell types and reprogramming methods, as reviewed by us and others (Pessôa et al. 2019a; Anwised et al. 2023). As for the application of those cells, due to its relevance as models, non-human primates are extensively studied, and iPSC-derived cardiomyocytes have shown to improve non-human primate heart function after heart injury, both allogenic or interspecies (Shiba et al. 2016, p. 201; Cheng et al. 2023) and recently, human iPSC-derived islets were used in the treatment of diabetic non-human primates (Du et al. 2022), amongst other relevant studies.
Hence, animal iPSCs play a crucial role in translational medicine, aiming at both human and veterinary applications. Large animal iPSCs, such as bovine or porcine, have been used as a biomedical model for human regenerative medicine due to their plasticity, becoming valuable tools for studying gametogenesis and embryo development, reproductive disease modeling, and other regenerative medicine applications.
In vitro gametogenesis from iPSCs: restoring and preserving the genetic inheritance
Gametogenesis is the process that germ cells undergo to generate a mature gamete (oocyte or sperm). It is a very sophisticated process and extremely difficult to recapitulate in vitro because of specific processes such as epigenetic reprogramming, including the global DNA demethylation, which allow these cells to pass genetic information correctly to the next generations. Much research has been done on the mechanisms and systems behind the development of germ cells, and in the last decade, many efforts have been made to understand and then reconstitute all these processes in vitro (in vitro gametogenesis, or IVG) (Surani and Hajkova 2010; Saitou and Yamaji 2012; Tang et al. 2016; Yoshimatsu et al. 2022).
The protocols for reconstituting gametogenesis using PSC have focused on the biological development and stem cell research in humans, since one of the main reasons for reconstituting all gametogenesis in vitro is to overcome infertility, such as aplasia of germ cells, non-obstructive azoospermia (NOA), and oocyte maturation failure syndrome. In farm animals, this technology has been pursued mostly because it allows an understanding of the processes of acquiring totipotency, and consequently, increasing the in vitro production of oocytes, as well as correcting reproductive disorders, and enhancing animal production and reproduction, especially in cattle and porcine, which are amongst the most important livestock species for milk and meat production (Mooyottu et al. 2011; Redel et al. 2019). Furthermore, studies on the production of in vitro embryos in porcine and cattle have already been used as models for humans since they more closely resemble the latter than rodents, especially during the initial development of in vitro embryos (Sjunnesson 2020). Moreover, this technology could potentially allow the preservation of endangered animals or even the generation of new individuals from non-conventional or even extinct animals, as long as there are viable cells (Saitou and Hayashi 2021; Seita et al. 2023).
The recent literature shows that the most efficient results with the generation of new offspring and fertile individuals have been reported in mice and rats (Hikabe et al. 2016; Oikawa et al. 2022). Based on the culture system described by other authors, Ishikura et al. (2021) successfully reconstituted the entire development of male germ cells from mouse ESCs (mESCs) in vitro (Ishikura et al. 2021). Consequently, both male and female gametes could be produced by mESCs in vitro using various strategies, which is advantageous for fundamental studies of germline development and clinical applications.
In humans, iPSCs were induced into PGCLCs and were aggregated using somatic cells from the mouse fetal ovary in a culture system called reconstituted ovaries (rOvary) (Irie et al. 2015; Sasaki et al. 2015; Yamashiro et al. 2020, p. 202). Oocyte-like cells (OLCs) were generated with gene expression profile similar to in vivo PGCs. However, the functionality of these cells in humans has not yet been proven (Yamashiro et al. 2018, 2020; Bharti et al. 2020), demonstrating the challenges in the generation of gametes.
It is already known that many regulatory and epigenetic mechanisms vary between species; for example, in mouse, during the specification process, BMP4 directly activates or does not activate the WNT signaling pathway, activating T cells. T cells directly activate Blimp1 and Prdm14. Thus, Prdm14 activates Tfap2C, which increases Blimp1 activity (Ohinata et al. 2009; Aramaki et al. 2013; Yao et al. 2022). In humans, Sox17 plays an essential role in the specification of PGCs (Irie et al. 2015; Yao et al. 2022). The BMP4 signaling pathway initially activates Sox17, while WNT activates Eomes; Blimp1 can be upregulated by Tfap2C, which is upregulated by Sox17 in response to the BMP4 signal (Yao et al. 2022).
Recently, Murase et al. (2024) induced epigenetic reprogramming and differentiation of human PGCLC pluripotent stem cells into pro-spermatogonia or mitotic oogonia. They demonstrated that BMP signaling is a key factor in the differentiation of hPGCLCs (Murase et al. 2024). Compared to mice and humans, monkeys exhibit distinct transcriptome dynamics following the transition from oogonia to the oocyte (Mizuta et al. 2022) and may use a distinct mechanism for oocyte differentiation, demonstrating that all discoveries related to the germline in mouse have facilitated studies of the generation of hPGCLCs or other species. However, these PGCLCs can be induced to haploid gametes in vitro, so further investigation is needed.
The derivation of follicular-like cells and oocytes has already been described in some species, such as porcine (Linher et al. 2009; Dyce et al. 2011) and bovine (de Souza et al. 2017), using ovarian and skin stem cells. In cattle, putative PGCLCs were generated from ESCs through different culture systems. The cells were positive to PRDM1/BLIMP1 proteins as well as TFAP2C, SOX17, OCT4, and NANOG, but not SOX2 (Shirasawa et al. 2024).
Our research group has reported preliminary results on the generation of porcine PGCLCs from iPSCs (Pieri et al. 2022) and also from cattle iPSCs (Bressan et al. 2018). The latter were analyzed for their pluripotency profile, epigenetic markers, the dynamics of genomic imprinting, miRNA profile, and global transcript analysis (FF Bressan, unpubl. data). Furthermore, we have already managed to generate bovine and porcine iPSCs from fetal fibroblasts and other non-invasive sources (urine), and these were differentiated into germline-like cells in vitro or germline-like cells (PGC-like or PGCLCs) (FF Bressan, K Recchia, NCG Pieri, unpubl. data).
However, the entire reconstitution of gametogenesis in vitro has yet to be reported in farm and domestic animals despite some ongoing work in bovine and swine. In pigs, we have used the rOvary culture system (Hayashi et al. 2012, p. 201; Hikabe et al. 2016; Bharti et al. 2020; Yamashiro et al. 2020) to obtain PGCLCs expressing pluripotency and germline genes OCT4, BLIMP1, PRDM14, and VASA, as well as REC8 (meiosis) and GDF9 (oocyte-specific) and FOXL2 (granulosa) (FF Bressan, NCG Pieri, unpubl. data).
Indeed, the generation of healthy offspring derived from in vitro germinative cells, so far, has only been shown in rodents. The production of functional germline and, eventually, gametes in vitro, sometimes called the ‘synthetic’ gametes, still has major drawbacks that are not evident for other cell lineages. The potential benefits of such differentiation range broadly from conservational purposes in endangered species to modeling inaccessible developmental stages in situ and reaching the cellular therapies used to surpass human infertility. On the other hand, the generation of gametes lacking an orchestrated epigenetic resetting may lead to unpredictable consequences during pregnancy and post-natal life, leading to important ethical questions to be discussed and still unknown boundaries to reach.
Cellular agriculture: the solution for sustainable animal-derived food
In vitro myogenesis is the process of acquiring mature muscle from the differentiation of mesenchymal stem cells (MSCs), progenitor cells, or pluripotent stem cells (PSCs) (Arnhold and Wenisch 2015; Świerczek et al. 2015; Al Tanoury et al. 2020). This process enables the study of muscle development and diseases in different species, as well as drug testing or gene therapy for genetic diseases such as Duchenne (Chal et al. 2015; Guan et al. 2020; Moretti et al. 2020). Furthermore, it allows the production of alternative protein via cell-cultured meat (Bhat et al. 2017; Treich 2021); this possibility has gained more space in both academia and industry.
Conventional meat production demands significant natural resources such as land and water, while also contributing to high greenhouse gas emissions and pollution (Guo et al. 2022; Muñoz-Ulecia et al. 2023). In contrast, alternative proteins require fewer natural resources compared to conventional meat and promote enhanced sustainability (Chriki and Hocquette 2020). Moreover, cell-cultured meat is engineered to mimic the sensory, nutritional, and structural characteristics of traditional meat, and this achievement remains a challenge, however, it represents a promising solution for the future of sustainable food production (Warner 2019). Scaling up production of these innovative technologies could play a crucial role in addressing the global challenge of feeding a growing population while minimizing environmental impact.
Scaling up the in vitro myogenesis is a challenge when derived from MSCs or progenitor due to their senescence. Consequently, the isolation of further cell lines through biopsies is needed, which could result in stress, pain, and medical treatment after the collection. Another option would be cellular immortalization (Stout et al. 2023). Moreover, using an immortalized cell line results in a transgenic cell, creating barriers for cellular agricultural. However, iPSCs can overcome this challenge, as they can be generated through non-integrative methods, and once reprogrammed into a pluripotent state, these cells can be maintained in culture without losing their plasticity (Yoshimatsu et al. 2021; Recchia et al. 2022; Zhu et al. 2023).
As previously discussed, iPSCs have been acquired from different animal species (Gonçalves et al. 2017; Pessôa et al. 2019b; Bressan et al. 2020; Machado et al. 2020); however, in vitro myogenesis derived from iPSCs has only been reported in murine (Hosoyama et al. 2014; Chal et al. 2016; Bruge et al. 2022) and human (Vu Hong et al. 2023). Chal et al. (2015) demonstrated the differentiation of hiPSCs into myotubes over a 30-day culture period. However, they observed a heterogeneous population. In 2023, Zhu and colleagues optimized this protocol for porcine PSCs, achieving a 3D tissue resembling meat when cells were cultured in a 3D scaffold. This promising outcome suggests potential for adaptation to other species, such as cattle, thereby enabling cellular agriculture to contribute to a promising and sustainable future (Zhu et al. 2023).
Conclusion and future perspectives
In veterinary medicine, generating pluripotent cells brings unique and essential benefits and numerous possible applications to each species of domestic and wild animals. For example, adequate biomedical models and disease modeling are generated from dogs, porcine, and non-human primates’ cell lineages, and farm animals are beneficiaries of the optimization of technology in precision farming, where several applications can be prospected, such as the generation of cultivated meat in a more sustainable production system, and, in particular, of reproductive applications, including the generation of functional gametes aimed to maximize animal production and reproduction, as well as the conservation of genetic resources and their dissemination.
In this context, the knowledge of the specific molecular pathways for the acquisition of toti- or pluripotency, as well as those related to the differentiation process, and the knowledge of the molecular pathways that drive the assertive reprogramming, are essential before critical applications of these stem cells can be validated for both medicine and farming purposes. Until today, however, these mechanisms have not been investigated in species other than human and mouse models. Challenges involve identifying the molecular mechanism that confers a unique identity on pluripotent and functional differentiated cells and using integration-free technologies to express transcription factors, such as chemical or episomal reprogramming.
Finally, the establishment of viable conditions and models will enable new possibilities in modulating cell phenotypes for practical use in medicine (e.g. modeling genetic diseases, cancer, or fertility purposes) and will prominently provide beneficial technologies for agriculture (e.g. optimization of herds, climate issues, etc.) and preservation and dissemination of the genetic material (for commercial or conservational purposes), enabling and enhancing the clinical and commercial potential of reprogramming technology, including the generation of viable and healthy offspring.
Data availability
Data sharing is not applicable as no new data were generated or analyzed during this study.
Declaration of funding
The authors would like to thank The Good Food Institute grant number 104416, CNPq (National Council for Scientific and Technological Development) and FAPESP (The São Paulo Research Foundation) for scholarships. The supporting sources were not involved in the preparation of the data or manuscript or the decision to submit for publication.
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