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Nogueira, I.P.M.; Costa, G.M.J.; Lacerda, S.M.D.S.N. Somatic Cell Sources for Reprogramming. Encyclopedia. Available online: https://encyclopedia.pub/entry/55741 (accessed on 15 April 2024).
Nogueira IPM, Costa GMJ, Lacerda SMDSN. Somatic Cell Sources for Reprogramming. Encyclopedia. Available at: https://encyclopedia.pub/entry/55741. Accessed April 15, 2024.
Nogueira, Iara Pastor Martins, Guilherme Mattos Jardim Costa, Samyra Maria Dos Santos Nassif Lacerda. "Somatic Cell Sources for Reprogramming" Encyclopedia, https://encyclopedia.pub/entry/55741 (accessed April 15, 2024).
Nogueira, I.P.M., Costa, G.M.J., & Lacerda, S.M.D.S.N. (2024, February 29). Somatic Cell Sources for Reprogramming. In Encyclopedia. https://encyclopedia.pub/entry/55741
Nogueira, Iara Pastor Martins, et al. "Somatic Cell Sources for Reprogramming." Encyclopedia. Web. 29 February, 2024.
Somatic Cell Sources for Reprogramming
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Induced pluripotent stem cells (iPSCs) were first generated by Yamanaka in 2006, revolutionizing research by overcoming limitations imposed by the use of embryonic stem cells. In terms of the conservation of endangered species, iPSC technology presents itself as a viable alternative for the manipulation of target genetics without compromising specimens.

induced pluripotent stem cells bird feather follicle cells somatic reprogramming germ cell

1. Introduction

According to the 2021 IUCN Red List, approximately 11,000 bird species are facing varying degrees of threat and risk to their populations [1]. Numerous projects worldwide aim to conserve these populations through measures based on environmental education, social mobilization, preservation and restoration of natural habitats, specimen monitoring, and in situ reproductive assistance [2][3][4][5]. However, in the face of animal trafficking, habitat destruction due to direct and indirect human actions, emerging diseases, natural disasters, and challenging reproductive rates, there remains a prevailing negative pressure on at-risk populations [2][5][6].
The pursuit of convenient assisted reproductive technology (ART) is driven by the intention to provide a genuine opportunity for these avian species to overcome the rate of destruction and effectively recover their populations [7]. There are two major cornerstones for ex situ species conservation: the requirements that populations be self-sustainable and that they maintain a degree of genetic diversity [8]. Approaches such as the use of gamete cryopreservation, which is already a bottleneck for avian female reproduction [9][10], and laboratory-dependent techniques such as in vitro fertilization (IVF) and even avian cloning do not fulfill these proposed basic principles [11]. Moreover, stem cell-based technologies, such as the utilization of embryonic stem cells (ESCs) or adult multipotent stem cells, also necessitate invasive collection procedures. The acquisition of these cells puts at risk the viability of embryos or even specimens from endangered populations, rendering it impractical considering conservation goals [12][13]. In addition to all that, the biosafety of reproductive techniques is a critical consideration, since the ultimate objective in conservation is the recovery of populations in their natural habitats. For instance, the somatic cell nuclear transfer (SCNT) method may raise scientific and ethical concerns due to the potential risks of abnormal offspring development, thereby hindering its suitability for conserving wild animals [8][14].

2. Somatic Cell Sources for Reprogramming

In avian species, although the entire embryo originates from the center of the epiblast and possesses remarkable regenerative abilities [13], manipulating a fertilized egg from an endangered species poses the risk of permanent contamination and definitive loss. Therefore, the utilization of pluripotent embryonic cells, such as chicken embryonic stem cells (cESCs) and chicken embryonic fibroblasts (CEFs), is deemed impractical for animal conservation research [12][15]. Additionally, due to the limited availability of post-hatch eggshells from wild species, avian amniotic stem cells, also known as amniotic fluid stem cells (AFSCs), may not be the optimal alternative for such studies [13].
In chickens, mesenchymal stem cells (cMSCs) have been isolated from various organs such as the liver, lung, and bone marrow. These cells have demonstrated the ability to differentiate into a wide range of cell types such as osteogenic, adipogenic, and endothelial [13][15][16]. However, collecting these cells in a noninvasive and feasible manner from healthy animals within their natural habitat also poses significant challenges.
Thus, the capacity to generate pluripotent cells via the genetic reprogramming of adult somatic cells has brought about a revolutionary shift in stem cell research, not only exerting a substantial impact on the fields of regenerative medicine and drug discovery but also providing a valuable instrument for conducting research using avian models. Notably, iPSCs opened new avenues for the exploration and implementation of ex situ reproduction projects [12][13][15][16].
The first crucial criterion for achieving successful reprogramming is determining the appropriate source of a somatic cell type for inducing pluripotency once it significantly influences efficiency, kinetics, and the quality of iPSC generation. Other important aspects to consider when selecting the somatic cell type include cell availability, the process of cell acquisition, the requirements for cell maintenance, and its reprogramming capacity, ensuring that the chosen cell type aligns with the specific research objectives [17]. Consequently, numerous research groups have investigated diverse somatic cell sources in order to identify promising candidates for reprogramming into iPSCs. These sources primarily encompass easily accessible adult cells that can be isolated noninvasively or minimally invasively, such as dermal fibroblasts and keratinocytes, urine cells, and peripheral blood mononuclear cells (PBMCs) [18].
In the case of mice, the initial reprogramming studies were performed using mouse embryonic fibroblasts (MEFs) and tail-tip fibroblasts (TTFs) [19], and subsequent studies successfully achieved reprogramming of adult human dermal fibroblasts (HDFs) [20][21]. Regarding avian iPSC production from somatic tissues, fibroblasts have been extensively used due to their abundance, ease of cultivation, and well-defined protocols [13]. Some research groups achieved successful derivation of avian iPSCs from embryonic fibroblasts [15][16][22][23]. However, as previously mentioned, it is crucial to ensure that the obtainment of donor cells does not compromise the viability of the individual specimen when considering their potential application in conservation efforts.
As an alternative, dermal fibroblasts have already been used to produce avian iPSCs [24][25][26]. Feathers are complex epidermal appendages that contain a pulp with a rich quantity of feather follicle cells (FFCs) of various types such as erythrocytes, keratinocytes, and dermal fibroblasts [25][27], which are one of the most recruited cell sources in avian iPSC derivation projects. These cells can be collected minimally invasively from birds by plucking feathers from the primary and secondary wing remiges [23][24][27]. Cell acquisition from the calamus pulp opening offers a simplified process for isolating skin cells through enzymatic and mechanical digestion, resulting in a high yield. Significantly, the quantity of tissue within the follicle exhibits variation based on the developmental stage of the feather, with nascent feathers exhibiting a greater abundance of pulp tissue [27]. Therefore, FFC obtainment in adult birds is performed in two steps. The first stage involves removing a mature feather, and after 15 to 20 days of first removal, a second assembly involves removing the reactivated calamus from the same feather, now containing a substantial amount of pulp tissue [27]. In a natural habitat, capturing the same bird consecutively presents a considerable challenge if not an impossibility. Therefore, an alternative approach involves collecting feathers from juvenile individuals that are still in the nest and undergoing the feathering phase, as they possess an actively developing pulp [23][27], potentially allowing for a single collection session to be sufficient. Another significant source of donor cells for reprogramming is dermal fibroblasts obtained from cutaneous tissue of recently deceased wild animals. Although under nonideal conditions, these cells demonstrated successful utilization in the generation of iPSCs of rare avian species [24]. As a potential strategy, these materials could also be collected in controlled environments, such as zoos during medical assessments [8], ensuring better sample quality and minimizing the risk of contamination.
In human medicine, fibroblasts have certain drawbacks that need to be considered when using them as a somatic cell source for generating human iPSCs (hiPSCs). These include the need for a skin biopsy, which can be undesirable; decreased reprogramming efficiency in aged patients; heterogeneity within fibroblast populations; and the risk of accumulating mutations due to their constant exposure to the environment [28][29]. This has led to research for alternative cell sources that meet specific criteria for biomedical applications. Keratinocytes have emerged as a promising cell source for hiPSC generation due to their accessibility. They can be alternatively obtained from hair follicles using noninvasive methods such as plucking a hair in the active growth phase. Reprogramming human keratinocytes to pluripotency has been achieved using retroviral transduction of Yamanaka factors (OCT4, SOX2, KLF4, and c-MYC - OSKM), resulting in higher efficiency, faster kinetics, and fewer retroviral integrations compared to fibroblast reprogramming due to their epithelial gene signature [18][28][30]. However, there are limitations to their use, such as fast senescence after a few passages and longer doubling time, requiring careful cultivation.
Xi and colleagues (2013), reported that keratinocytes obtained from the internal epidermal layer of the feather follicle of adult White Leghorn chickens exhibit characteristics of multipotent stem cells. Chicken keratinocytes can be separated in vitro from the FFC fibroblasts, as the latter quickly attach to culture plates within 2 h, while keratinocytes take about 24 h to attach [25][27]. These cells were shown to be highly efficient in incorporating foreign genes, surpassing fibroblast-like cells, and displaying elevated levels of exogenous gene expression [25], highlighting the importance of feather keratinocytes in enabling genetic engineering techniques for endangered avian species.
In addition to the use of keratinocytes for human iPSCs, urine cells offer a noninvasive means of collection that does not require professional assistance, making it readily accessible compared to other cell sources. Although urine cells consist of a heterogeneous population, successful reprogramming into hiPSCs has been achieved using both integrating and nonintegrating methods [31]. They naturally express stem cell-specific genes and surface markers associated with pluripotency, and their epithelial nature does not require them to undergo the mesenchymal-to-epithelial transition (MET) during reprogramming, leading to enhanced efficiency and kinetics [18][31][32]. Nevertheless, generating avian iPSCs from urine cells has never been accomplished. A plausible explanation for not using these cells in birds may be that it is impracticable to collect the urine of wild animals, as it would require the scientist to be present at the exact moment of excretion. Additionally, the avian urinary system shares the same pathway as the digestive system [33], raising concerns about potential sample contamination with intestinal content and microorganisms.
Another major source of hiPSCs are the peripheral blood mononuclear cells (PBMCs), which consist of various cell types, including lymphocytes, monocytes, dendritic cells, natural killer cells, and hematopoietic stem cells/progenitor cells. They offer several advantages as a somatic cell source for generating hiPSCs as they are highly proliferative and reprogrammable using viral-based techniques and integration-free approaches [18][34][35]. At present, there are no reports of avian PBMC-derived iPSCs. Since it is considered to be minimally invasive, blood collection from zoo animals or research animals could be used in tests for bird iPSC derivation. It would be of interest to investigate the behavioral characteristics of avian nucleated erythrocytes during the reprogramming process.
Many somatic cell types have yet to be investigated for avian iPSC generation. Thus, future research should aim to validate the existence of more efficient and viable cellular sources for conservation applications in endangered species, surpassing the fibroblasts used by most research groups. Divergent physiological characteristics between avian and mammalian species manifest across several key parameters. Avian cells exhibit a significantly lower cellular basal metabolism, attributable to a concomitant reduction in mitochondrial lipid content and oxygen consumption. Additionally, avian cells demonstrate lower membrane polyunsaturation and diminished total antioxidant capacity compared to their mammalian counterparts [36]. These features may bear noteworthy implications for the reprogramming of primary somatic cells into iPSCs. The cellular metabolic rate has the potential to alter the kinetics and velocity of the reprogramming process, while disparities in oxidative stress parameters, such as lower basal cellular oxygen consumption and reduced lipid oxidative damage in avian cells, could impact the redox state and overall stress response of cells, thereby influencing the success of iPSC generation. Significantly, long-lived species in both avian and mammalian groups present intriguing distinctions, with fibroblasts from avian species exhibiting delayed yet prolonged phosphorylation of ERK [37], which could interfere not only in the acquisition of a pluripotent state but also in its maintenance.
Despite these observations, there is a notable absence of studies comparing the efficiency of the reprogramming process and the quality of iPSCs generated from avian, murine, and human somatic cells. Compounding this gap in knowledge are substantial differences, such as the higher core temperatures exhibited by avian species (ranging between 34 and 44 °C) in contrast to their mammalian counterparts (with core temperatures ranging between 30 °C and 40 °C), despite being subjected to similar cultivation conditions [38].
For chicken cells, research groups have expanded fibroblasts in Kuwana’s modified avian culture medium-1 (KAV-1) containing chicken serum [24]. However, despite cellular differences in metabolism, primary cultures of fibroblasts from mice, humans, and birds are carried out in a remarkably similar manner, utilizing Dulbecco’s modified Eagle’s medium (DMEM) with 10% fetal bovine serum (FBS) at an incubation temperature of 37 degrees Celsius and 5% CO2 [20][26][39][40][41]. Acknowledging these physiological nuances is imperative for refining reprogramming strategies and ensuring the optimization of culture conditions and growth factors specific to avian cells. The intricate interplay between avian-specific physiological traits and the reprogramming process warrants further exploration to advance the field of avian iPSC research.

3. Reprogramming Factors

Yamanaka and colleagues successfully reprogrammed somatic cells of mice and humans based on the overexpression of the four defined transcription factors: Oct3/4 (also known as Pou5f1), Sox2, Klf4, and c-Myc [19][20][41][42][43]. Rosselló and colleagues (2013) demonstrated that human OSKM genes are capable of deriving iPSCs not only in vertebrates, e.g., Galliformes, but also in invertebrates, providing evidence for the conservation of reprogramming pathways between different species [8][44].
The regulatory circuitry among these factors exhibits interconnectivity and feed-forward regulation. In ESCs, Oct4, Sox2, and Klf4 were found to autoregulate, as the latter was observed to enhance the role of Oct4 and Sox2 in developmental pathways. c-Myc did not exhibit such a pattern as it is not autoregulated and plays a distinct role in metabolic processes of cells undergoing reprogramming [42][45][46]. Yamanaka factors have the capability to regulate well-established ESCs’ pluripotency-associated signaling pathways, including p53, Wnt, TGF-b, Hedgehog, and MAPK pathways, through various combinations [20]. Both Oct4 (octamer-binding transcription factor 4) and Sox2 (sex-determining region Y-box 2) have overlapping functions in the regulation of gene expression networks associated with a role of pluripotency maintenance. Dysregulation of these gene expressions leads to loss of pluripotency and cell differentiation [45][47]. The mouse Oct4 gene was identified in chickens as cPouV, showing similarities to mammalian OCT4 orthologues [45].
Klf4 (Kruppel-like factor 4) was found to be involved in direct somatic reprogramming of fibroblasts into iPSCs, specifically in regulating pluripotency-associated genes such as Klf2 and Klf5 [16][45][48]. c-Myc, on the other hand, is considered a nonessential factor in iPSC generation, as in its absence, iPSCs can still be generated. However, c-Myc expression is essential for high-quality iPSCs due to its role in controlling histone acetylation [46][49].
In a complementary manner, certain genes, particularly Nanog and Lin28, were identified as enhancers for improving the efficiency of iPSC reprogramming in humans and birds [42][47][50][51]. Nanog (Nanog Homeobox) is a transcriptional factor, controlled by Oct4 and Sox2 in rewiring transcriptional networks to promote self-renewal and suppress differentiation by finely modulating epigenetic remodeling. Once Nanog is inactivated, the iPSCs differentiate into endoderm-like cells [50][51][52]. Lin28 encodes an RNA-binding protein that regulates the let-7 family of microRNA, which controls genes related to differentiation and growth. Thus, Lin28 plays an important role not only in early embryo development but also in regulating reprogramming, naive/primed pluripotency, and stem cell metabolism [53][54]. One of the pioneering studies in domestic birds demonstrated successful reprogramming of avian embryonic fibroblasts transduced with six human reprogramming factors: POU5F1, NANOG, SOX2, LIN28, c-MYC, and KLF4 [16].
A major challenge in generating iPSCs from wild avian species is the need for specific reprogramming genes, hampering the standardization of the induction protocol. A recent study revealed a significant demand for reprogramming wild avian FFCs. A transposon vector carrying eight mouse reprogramming factors (Oct3/4, Sox2, Klf4, c-Myc, Klf2, Lin28, Nanog, and Yap) had to be employed to achieve a full pattern of reprogrammed Japanese golden eagle cells [24]. Activation of Yap/Taz was implicated in the reprogramming of mouse somatic cells into tissue-specific stem/progenitor cells as well as in the reprogramming of human adult cells into iPSCs [55]. Yap (yes1-associated transcriptional regulator) plays a significant role in the cellular expansion, self-renewal, and maintenance of the stem cell phenotype by participating in metabolic rearrangement to meet the changes in bioenergetic and biosynthetic demands [55][56].
Yap assumes a role marked by complexity and controversy. Despite its recognized promotion of stemness in various stem cell types, including pluripotent stem cells, its impact extends to the early determination of cell fate and differentiation, concurrently opposing pluripotency during the initial stages of embryogenesis [57][58][59]. This dual modality contributes to the intricate and occasionally contradictory nature of Yap engagement in pluripotency regulation, wherein it inhibits pluripotency induction autonomously within cells while concurrently fostering it in a non-cell-autonomous manner through microenvironmental alterations [58]. Given these complexities, further investigation into the specific effects of Yap in avian reprogramming processes would be valuable for a comprehensive understanding of its role in diverse biological contexts.
As a result, research efforts pertaining to each target species must be conducted in a unique and individual manner. This approach will ensure that species-specific considerations are considered, optimizing the success and efficiency of high-quality iPSC generation for each particular avian species.

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