Dermal Stem Cells Research Articles

Advances in dermal melanocytes

Dermal stem cells(DSCs)have great proliferation and multidirectional differentiation potential. Keratinocytes can induce DSCs to migrate and differentiate into melanocytes by expressing Wnt-3a and E-cadherins. Researches have indicated that the generation of dermal and epidermal melanocytes is dependent on different signaling pathways. More concretely, epidermal melanocyte generation is highly dependent on the stem cell factor(SCF)signaling pathway, while dermal melanocyte generation on the endothelin 3(ET3)and hepatocyte growth factor(HGF)signaling pathways. The origin of nevus cells in pigmented nevus is not yet clear. Some studies suggest that nevus cells may derive from the stem cells which can differentiate into melanocytes. DSCs can differentiate into melanocytes, but further research is needed to determine whether they are the source of nevus cells. Key words: Melanocytes; Dermis; Signal transduction; Nevus, pigmented; Epidermis

Activation and regulation of the granulation tissue derived cells with stemness-related properties.

IntroductionSkin as the largest and easily accessible organ of the body represents an abundant source of adult stem cells. Among them, dermal stem cells hold great promise in tissue repair and the skin granulation tissue has been recently proposed as a promising source of dermal stem cells, but their biological characteristics have not been well investigated.MethodsThe 5-bromo-2′-deoxyuridine (BrdU) lineage tracing approach was employed to chase dermal stem cells in vivo. Granulation tissue derived cells (GTCs) were isolated and their in vitro proliferation, self-renewing, migration, and multi-differentiation capabilities were assessed. Combined radiation and skin wound model was used to investigate the therapeutic effects of GTCs. MicroRNA-21 (miR-21) antagomir was used to antagonize miR-21 expression. Reactive oxygen species (ROS) were scavenged by N-acetyl cysteine (NAC).ResultsThe quiescent dermal stem/progenitor cells were activated to proliferate upon injury and enriched in granulation tissues. GTCs exhibited enhanced proliferation, colony formation and multi-differentiation capacities. Topical transplantation of GTCs into the combined radiation and skin wound mice accelerated wound healing and reduced tissue fibrosis. Blockade of the miR-21 expression in GTCs inhibited cell migration and differentiation, but promoted cell proliferation and self-renewing at least partially via a ROS dependent pathway.ConclusionsThe granulation tissue may represent an alternative adult stem cell source in tissue replacement therapy and miR-21 mediated ROS generation negatively regulates the stemness-related properties of granulation tissue derived cells.Electronic supplementary materialThe online version of this article (doi:10.1186/s13287-015-0070-9) contains supplementary material, which is available to authorized users.

Senescence of human skin-derived precursors regulated by Akt-FOXO3-p27(KIP¹)/p15(INK⁴b) signaling.

Multipotent skin-derived precursors (SKPs) are dermal stem cells with the capacity to reconstitute the dermis and other tissues, such as muscles and the nervous system. Thus, the easily available human SKPs (hSKPs) hold great promises in regenerative medicine. However, long-term expansion is difficult for hSKPs in vitro. We previously demonstrated that hSKPs senesced quickly under routine culture conditions. To identify the underlying mechanisms so as to find an effective way to expand hSKPs, time-dependent microarray analysis of gene expression in hSKPs during in vitro culture was performed. We found that the senescence of hSKPs had a unique gene expression pattern that differs from reported typical senescence. Subsequent investigation ruled out the role of DNA damage and classical p53 and p16(INK4a) signaling in hSKP senescence. Examination of cyclin-dependent kinase inhibitors revealed the involvement of p15(INK4b) and p27(KIP1). Further exploration about upstream signals indicated the contribution of Akt hypo-activity and FOXO3 to hSKP senescence. Forced activation of Akt and knockdown of FOXO3, p15(INK4b) and p27(KIP1) effectively inhibited hSKP senescence and promoted hSKP proliferation. The unique senescent phenotype of human dermal stem cells and the role of Akt-FOXO3-p27(KIP1)/p15(INK4b) signaling in regulating hSKP senescence provide novel insights into the senescence and self-renewal regulation of adult stem cells. The present study also points out a way to propagate hSKPs in vitro so as to fulfill their promises in regenerative medicine.

Hair follicle dermal stem cells regenerate the dermal sheath, repopulate the dermal papilla, and modulate hair type.

The dermal papilla (DP) provide instructive signals required to activate epithelial progenitors and initiate hair follicle regeneration. DP cell numbers fluctuate over the hair cycle, and hair loss is associated with gradual depletion/atrophy of DP cells. How DP cell numbers are maintained in healthy follicles remains unclear. We performed in vivo fate mapping of adult hair follicle dermal sheath (DS) cells to determine their lineage relationship with DP and found that a subset of DS cells are retained following each hair cycle, exhibit self-renewal, and repopulate the DS and the DP with new cells. Ablating these hair follicle dermal stem cells and their progeny retarded hair regrowth and altered hair type specification, suggesting that they function to modulate normal DP function. This work identifies a bipotent stem cell within the adult hair follicle mesenchyme and has important implications toward restoration of hair growth after injury, disease, and aging.

Isolation and multiple differentiation potential assessment of human gingival mesenchymal stem cells.

The aim of this study was to isolate human mesenchymal stem cells (MSCs) from the gingiva (GMSCs) and confirm their multiple differentiation potentials, including the odontogenic lineage. GMSCs, periodontal ligament stem cells (PDLSCs) and dermal stem cells (DSCs) cultures were analyzed for cell shape, cell cycle, colony-forming unit-fibroblast (CFU-F) and stem cell markers. Cells were then induced for osteogenic and adipogenic differentiation and analyzed for differentiation markers (alkaline phosphatase (ALP) activity, mineralization nodule formation and Runx2, ALP, osteocalcin (OCN) and collagen I expressions for the osteogenic differentiation, and lipid vacuole formation and PPARγ-2 expression for the adipogenic differentiation). Besides, the odontogenic differentiation potential of GMSCs induced with embryonic tooth germ cell-conditioned medium (ETGC-CM) was observed. GMSCs, PDLSCs and DSCs were all stromal origin. PDLSCs showed much higher osteogenic differentiation ability but lower adipogenic differentiation potential than DSCs. GMSCs showed the medial osteogenic and adipogenic differentiation potentials between those of PDLSCs and DSCs. GMSCs were capable of expressing the odontogenic genes after ETGC-CM induction. This study provides evidence that GMSCs can be used in tissue engineering/regeneration protocols as an approachable stem cell source.

Three-dimensional hydrogel scaffolds facilitate in vitro self-renewal of human skin-derived precursors

Skin-derived precursors (SKPs) are multipotent cells with dermal stem cell properties. These easily available cells possess the capacity to reconstitute the skin in vivo, as well as a broader differentiation potential in vitro, which endows them with great prospects in regenerative medicine. However, the present authors’ group and others previously found that adult human SKPs (hSKPs) expanded deficiently in vitro, which largely counteracted their research and practical values. Taking the physiological micro-environment of hSKPs into consideration, the authors sought to establish a hydrogel scaffold-based three-dimensional (3-D) culture system for hSKPs in the present study. After comparing their morphology, growth characteristics, signature gene expression and differentiation potential in different hydrogels, the present authors found that a chemically defined hyaluronic acid and denatured collagen-based hydrogel system that mimicked the natural niche of hSKPs in the dermis could alleviate hSKP senescence, support hSKP proliferation as spheres, while largely retaining their properties and potential. This study suggested that recapitulating the in vivo stem cell niche by providing them with 3-D extracellular matrix environments could help them achieve better self-renewal in vitro. In addition, the animal-origin-free and biocompatible 3-D hydrogel system will certainly benefit fundamental research and clinical applications of hSKPs in the near future.

Стволовые клетки кожи как объект криоконсервирования. 1. Стволовой резерв кожи

The review contains the data on scope, properties and localization of resident stem/progenitor cells of skin. The emphasis is given to populations of epithelial and dermal stem cells (SCs), as well as of melanocyte and subcutaneous fat SCs. The cells represent a prospective object for cryobiological technologies and establishing low temperature banks for use in theoretical and experimental biology, general and personalized medicine, development of bioengineered equivalents of tissues and artificial organs. Probl Cryobiol Cryomed 2014; 24(1):3–15.

Melanocyte stem cells and malignant melanoma

Malignant melanoma is a highly metastatic cancer resistant to conventional therapy.The development of melanoma involves both genetic and environmental factors.Most cases of melanoma arise de novo,but some are known to arise in preexisting melanocytic nevi.The traditional hypothesis for melanoma development is that cutaneous melanocytes progressively accumulate mutations in oncogenes and tumor suppressor genes over a long time during exposure to ultraviolet,leading to uncontrolled proliferation of melanocytes with acquisition of invasive and metastatic properties,and finally resulting in melanoma formation.An alternative hypothesis is that melanoma begins in extrafollicular dermal melanocyte stem cells (MSCs).Ultraviolet-induced mutations may cause the development of melanoma by altering the process of self-renewal,expansion and differentiation of normal MSCs.Understanding the mechanism underlying melanoma development is conducive to its treatment. Key words: Melanoma; Melanocytes; Stem cells

Promise of Human Induced Pluripotent Stem Cells in Skin Regeneration and Investigation

Induced pluripotent stem cell (iPSC) technology has initiated a new era in biomedical science. The skin has been realized as an ideal platform for iPSC applications; unlike other organs, the skin is easily accessible, highly proliferative, and reconstitutable. Currently, skin equivalents can be generated from iPSCs not only from healthy individuals but also from patients with genodermatoses, providing novel platforms for dissecting disease pathophysiology and establishing cell-based therapy. With their developmental plasticity, iPSCs may also enable the regeneration of skin appendages. The iPSC technology may provide novel remedies for intractable disorders, once key issues particularly, safety concerns, are cleared.

Effect of human dermal mesenchymal stem cells on the expression and secretion of interleukin-13 by perilesional CD8+ T lymphocytes from patients with vitiligo

Objective To evaluate the effect of human dermal mesenchymal stem cells (DMSCs) on the expression and secretion of interleukin (IL)-13 by perilesional CD8+ T lymphocytes from patients with vitiligo.Methods Tissue specimens were obtained from the perilesional region of six patients with active vitiligo,and CD8+ T lymphocytes were isolated from both the tissue specimens and peripheral blood of these patients.DMSCs and melanocytes were obtained from the foreskin tissue of healthy males.The 3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium,inner salt (MTS) assay was performed to estimate the effect of different concentrations of recombinant IL-13 on the proliferation of melanocytes,reverse transcripition-PCR and Western blotting to detect the mRNA and protein expressions of IL-13 in perilesional and peripheral blood CD8+ T lymphocytes respectively,real-time quantitative reverse transcription (RT)-PCR and enzyme-linked immunosorbent assay (ELISA) to detect the IL-13 mRNA expression in,and IL-13 protein expression in the culture supematant of,CD8+ T lymphocytes before and after coculture with DMSCs,respectively.Statistical analysis was done by t test.Results No obvious changes were observed in the proliferation of melanocytes treated with different concentrations (10,50,100,250,500 μg/L) of recombinant IL-13 for various durations (24,48,72 and 96 hours)compared with untreated melanocytes (all P ＞ 0.05).Both perilesional and peripheral blood CD8+ T lymphocytes expressed IL-13,and the expression was stronger in perilesional than in peripheral blood CD8+ T lymphocytes.A significant decrease was noted in IL-13 mRNA expression (0.100 0 ± 0.002 4 vs.0.383 2 ± 0.018 7,P ＜ 0.05) and protein level in the culture supernatant ((1 509.62 ± 48.44) ng/L vs.(5 507.98 ± 34.11) ng/L,P ＜ 0.05) of CD8+ T lymphocytes cocultured with DMSCs compared with monocultured CD8+ T lymphocytes.Conclusions There is a strong expression of IL-13 by perilesional CD8+ T lymphocytes in patients with vitiligo,which may be inhibited by DMSCs and serve as a target for the treatment of vitiligo. Key words: Vitiligo; CD8-positive T-lymphocytes; Mesenchymal stem cells; Interleukin-13

Bone morphogenetic proteins 4 and 2/7 induce osteogenic differentiation of mouse skin derived fibroblast and dermal papilla cells

Heterotopic ossification is a pathological condition in which bone forms outside the skeletal system. It can also occur in skin, which is the case in some genetic disorders. In addition to precursor cells and the appropriate tissue environment, heterotopic ossification requires inductive signals such as bone morphogenetic proteins (BMP). BMPs are growth and differentiation factors that have the ability to induce cartilage and bone formation in ectopic sites. The objective of this study is to explore the effect of the BMP-4 homodimer and BMP-2/7 heterodimer on the osteogenic differentiation of primary mouse skin fibroblasts and hair follicle dermal papilla (DP) cells. Osteogenic differentiation was induced by osteogenic induction medium (OS) containing 10 nM dexamethasone. The effect of BMP-4 and BMP-2/7 was studied using alkaline phosphatase (ALP) and calcium assays after 1.5, 3 and 5 weeks of differentiation. Fibroblasts and DP cells were able to differentiate into osteoblast-like matrix mineralizing cells. The first visible sign of differentiation was the change of morphology from rounded to more spindle-shaped cells. BMP-4 and BMP-2/7 exposure elevated ALP activity and calcium production significantly more than OS alone. The osteogenic response to BMP-4 and BMP-2/7 was similar in fibroblasts, whereas, in DP cells, BMP-2/7 was more potent than BMP-4. OS alone could not induce osteogenic differentiation in DP cells. Clear and consistent results show that dermal fibroblasts and stem cells from the dermal papilla were capable of osteogenic differentiation. The BMP-2/7 heterodimer was significantly more effective on hair follicular dermal stem cell differentiation.

Pathological niche environment transforms dermal stem cells to keloid stem cells: A hypothesis of keloid formation and development

Keloid is a disease that is difficult to cure because of its high recurrence rate after chemotherapy or radiotherapy, therefore it is considered as a benign skin tumor. Tumor stem cells are proposed as the source for tumor development and post-therapy recurrence. Interestingly, keloid stem cells have also been discovered, which share some characters with those of skin progenitor cells. Keloid patients possess specific diathesis including genetic predisposition and gene mutation, abnormal levels of hormones, growth factors and cytokines, and strong inflammatory response. This article reviews related literatures and hypothesizes that keloid stem cells might be transformed from normal dermal progenitor cells in the pathological niche of keloid tissues. These keloid stem cells are highly self-renewal and drug resistant, and can sustain themselves by asymmetric division, and continually generate new keloid cells to replenish the cells killed by drugs or radiation, thus leading to over growth of keloid and high post-therapy recurrence rate.

Comparison between fibroblasts and mesenchymal stem cells derived from dermal and adipose tissue

Stem cells have the ability to renew themselves and differentiate into various cell types. For this reason, numerous research groups have been studying these cells for their therapeutic potential. Some of the therapies, however, are not producing the expected results because of contamination by other cell types, especially by fibroblasts. In the cosmetic industry, stem cells are used to test the efficacy of anti-ageing and rejuvenation products. The purpose of this work was to gain a better understanding of the differences in phenotype, in gene expression associated with stem cells, in the pattern of cell surface proteins and in the differentiation capacity of adipose-derived stem cells, of skin-derived stem cells and of commercially available fibroblasts. In this study, we compared fibroblasts with mesenchymal stem cells derived from bone marrow, skin (dermis) and adipose tissue, to assess the differentiation potential of fibroblasts. Dermal and adipose stem cells were isolated from aesthetic surgery patients, and fibroblasts were obtained from a commercial source. The following parameters were used in this study: immunophenotypic profile (positive: CD29, CD73, CD90 and CD105; negative: CD14, CD45 and HLA-DR); differentiation into osteoblastic, chondrogenic and adipogenic cell types; and PCR array to analyse the gene expression of cells isolated from different culture passages. Fibroblasts express the same cell immunophenotypic markers, as well as the genes that are known to be expressed in stem cells, and were shown to be expressed also in adipose and dermis stem cells. Fibroblasts are also able to differentiate into the three cell lineages mentioned above, that is, adipocytes, osteocytes and chondrocytes. Human dermal fibroblasts have a potential to adhere to plastic surfaces and differentiate into other cell types. However, for stem cells intended to be used in cosmetics, experiments conducted with contaminated fibroblasts may produce poor or even falsely negative results for the efficacy of the active ingredient or formulation and thus conceal their promising effects as anti-ageing and skin rejuvenation products.

Differentiation of Human Dermal Mesenchymal Stem Cells into Cardiomyocytes by Treatment with 5-Azacytidine: Concept for Regenerative Therapy in Myocardial Infarction

Myocardial infarction (MI) is the leading cause of death worldwide. Stem cells regenerative medicine offers a promising approach to cure such degenerative disorders. Mesenchymal stem cells are thought to be one of the important types of stem cells which can differentiate into various lineages such as neuron, hepatocytes, and cardiomyocytes. In the present study, human dermal mesenchymal stem cells (hDMSCs) have been developed from human scalp punch biopsy and characterized for their mesenchymal phenotype so that these cells can be useful for differentiating into cardiomyocytes. 5-Azacytidine induces cardiomyocyte differentiation in vitro and therefore it has been used to differentiate hDMSCs cells into cardiomyocytes. It was observed that hDMSCs differentiated into cardiomyocyte within a period of 4 days to 15 days after treatment with 10 μM and 20 μM of 5-azacytidine. The cardiomyocyte phenotype was confirmed by studying expression of α-cardiac actin, β-myosin heavy chain, and cardiac troponin T. Thus, this paper describes the differentiation of hDMSCs into cardiomyocytes which can be further be used for treatment of MI. This type of cell-based cardiac therapy will offer a new hope for millions of patients worldwide who are suffering from heart disease.

Enrichment and Characterization of Human Dermal Stem/Progenitor Cells by Intracellular Granularity

Adult stem cells from the dermis would be an attractive cell source for therapeutic purposes as well as studying the process of skin aging. Several studies have reported that human dermal stem/progenitor cells (hDSPCs) with multipotent properties exist within the dermis of adult human skin. However, these cells have not been well characterized, because methods for their isolation or enrichment have not yet been optimized. In the present study, we enriched high side scatter (SSC(high))-hDSPCs from normal human dermal fibroblasts using a structural characteristic, intracellular granularity, as a sorting parameter. The SSC(high)-hDSPCs had high in vitro proliferation properties and expressed high levels of SOX2 and S100B, similar to previously identified mouse SOX2+ hair follicle dermal stem cells. The SSC(high)-hDSPCs could differentiate into not only mesodermal cell types, for example, adipocytes, chondrocytes, and osteoblasts, but also neuroectodermal cell types, such as neural cells. In addition, the SSC(high)-hDSPCs exhibited no significant differences in the expression of nestin, vimentin, SNAI2, TWIST1, versican, and CORIN compared with non-hDSPCs. These cells are therefore different from the previously identified multipotent fibroblasts and skin-derived progenitors. In this study, we suggest that hDSPCs can be enriched by using characteristic of their high intracellular granularity, and these SSC(high)-hDSPCs exhibit high in vitro proliferation and differentiation potentials.

A study on the activity of dermal multipotent stem cells in initiation of wound repair

Background: Wound healing is a process of cell-cell interaction and cell-extracellular matrix interaction. Dermal multipotent stem cells (dMSCs) have the abilities to promote survival and wound healing, but the potential function of dMSCs in wound healing, particularly in the initiation of wound repair, has not been fully understood. Methods: dMSCs and fibroblasts were isolated from neonatal rat dermis and were further purified and expanded. The cell cycles were determined with flow cytometry, while the radiosensitivity was measured by MTT assay. Rats were wounded with a 7-cm incision on the back skin and the wound fluids were collected by inserting two pieces of sterile polyvinyl alcohol sponge (1 cmin diameter and0.4 cmin thickness) subcutaneously into the dorsum of each rat through the midline of incision on the 1st, 2nd, 3rd and 4th day after incision. The effects of wound fluids on the proliferation of dMSCs and fibroblasts were measured with MTT assays. dMSC’s abilities of adhesion and attachment and its migration in response to wound fluids collected on the 1st day after incision were explored by measuring the percentage of floating cells and the cells migrated into wounding area in vitro, respectively. Results: The isolated dMSCs were morphologically homogenous and highly proliferative. Most of the cultured dMSCs were quiescent with few apoptotic cells. Compared with fibroblasts, dMSCs were more sensitive to radiation and more proliferative in response to wound fluids, especially to the wound fluids collected on the 1st day after wounding. Moreover, their abilities to attach, adhere and migrate were significantly enhanced with the early-phase wound fluids. Conclusions: As primitive stem cells, dMSCs are very responsive to wound fluids, which suggests dMSCs’ important role in wound healing, especially in initiating wound repair.

Stem cells and the skin

Stem cells live long lives, renew themselves, and differentiate into more mature, less potent, specialized cells, such as epidermal keratinocytes and dermal fibroblasts. Stem cells can be embryonic, if derived from an embryo, or adult/somatic if derived from postembryonic tissue. By producing new skin cells, stem cell division and differentiation can potentially rejuvenate skin and restore hair. To reproduce, stem cells can undergo symmetric nondifferentiative or differentiative divisions, or asymmetric differentiative divisions. Asymmetric divisions reproduce the stem cell and provide a more differentiated, but less potent transient amplifying cell. Divisions and differentiation of transient amplifying cells regenerate tissues by producing cells of a specific lineage, for example, keratinocytes. Epidermal stem cells lie in niches in the interfollicular epidermis, sebaceous gland, and in the bulge regions of hair follicles. These epidermal stem cells renew the epidermis, the sebaceous glands, and hair follicles after mature cells die. Dermal stem cells lie in the hair papillae, around pericytes, and elsewhere among other dermal cells. These form pericytes, myoblasts, fibroblasts, chondrocytes, and other specialized dermal cells. Along with other signaling pathways, the Wnt signaling pathway controls stem cell fate. Wnt signals enlist two functionally and chemically different gene coactivators to direct the time and type of replicative divisions. Stem cells may help to heal wounds, repair damaged tissues, regenerate aged skin, and reinvigorate growth of skin, hair, nails, and mucous membranes.

Dermal Stem Cells Can Differentiate Down an Endothelial Lineage

In this study, we have demonstrated that cells of neural crest origin located in the dermal papilla (DP) exhibit endothelial marker expression and a functional activity. When grown in endothelial growth media, DP primary cultures upregulate expression of vascular endothelial growth factor receptor 1 (FLT1) mRNA and downregulate expression of the dermal stem cell marker α-smooth muscle actin. DP cells have demonstrated functional characteristics of endothelial cells, including the ability to form capillary-like structures on Matrigel, increase uptake of low-density lipoprotein and upregulate ICAM1 (CD54) in response to tumour necrosis factor alpha (TNF-α) stimulation. We confirmed that these observations were not due to contaminating endothelial cells, by using DP clones. We have also used the WNT1cre/ROSA26R and WNT1cre/YFP lineage-tracing mouse models to identify a population of neural crest-derived cells in DP cultures that express the endothelial marker PECAM (CD31); these cells also form capillary-like structures on Matrigel. Importantly, cells of neural crest origin that express markers of endothelial and mesenchymal lineages exist within the dermal sheath of the vibrissae follicle.

Les deux visages de p63, Janus de la famille p53

The TP53 family member TP63 encodes two main isoforms TAp63 and ΔNp63 with distinct, often opposite functions during development and in the adult. ΔNp63 is crucial for the formation of the ectodermal derivatives and epidermis, while TAp63 is essential for heart development. In the adult, ΔNp63 behaves as a cell survival factor, controlling cell proliferation, adhesion and cell differentiation. In contrast, TAp63 is a proapoptotic factor that protects oocytes from genotoxic insults and prevents premature aging of dermal stem cells. In agreement with these activities, TAp63 is often lost and ΔNp63 overexpressed in cancer cells. Because of their opposite and competitive effects, p63 isoforms could be viewed as Janus two faces. The review focuses on the accumulating data on the p63 functions and regulation in the last decade.

Autophagy in Myocardial Differentiation and Cardiac Development

Autophagy represents an important biological process that contributes to cellular homeostasis. It is induced when the cell experiences stress, including nutrient and energy deprivation. For instance, the absence of nutrients and growth factors induces autophagy within minutes.1 Autophagy functions to protect cells against potential damage in association with exposure to stress, and thereby helps to defend cells and, subsequently, organs against dysfunction. There are multiple lines of evidence that autophagy has disease-preventing effects and, if disease still occurs, autophagy may limit disease severity.2 In addition, autophagy appears to play a key role in delaying the aging process.3,4 Article, see p e29 How does autophagy mediate such disease-preventing and disease-limiting effects? For damage control, cells generate double-membrane vesicles, called autophagosomes, which sequester portions of the cytosol, including proteins and organelles. After fusion of an autophagosome with a lysosome, the sequestered cytosolic contents are degraded. This process allows cells to eliminate and recycle …