The Epigenetic Regulation of Quiescent in Stem Cells

Mehran Radak; Hossein Fallahi

doi:10.1055/s-0043-1777072

Global Medical Genetics, Inhaltsverzeichnis

CC BY 4.0 · Glob Med Genet 2023; 10(04): 339-344
DOI: 10.1055/s-0043-1777072

Review Article

The Epigenetic Regulation of Quiescent in Stem Cells

Mehran Radak

¹Department of Biology, School of Sciences, Razi University, Baq-e-Abrisham, Kermanshah, Islamic Republic of Iran

,

Hossein Fallahi

¹Department of Biology, School of Sciences, Razi University, Baq-e-Abrisham, Kermanshah, Islamic Republic of Iran

› Institutsangaben

Abstract

This review article discusses the epigenetic regulation of quiescent stem cells. Quiescent stem cells are a rare population of stem cells that remain in a state of cell cycle arrest until activated to proliferate and differentiate. The molecular signature of quiescent stem cells is characterized by unique epigenetic modifications, including histone modifications and deoxyribonucleic acid (DNA) methylation. These modifications play critical roles in regulating stem cell behavior, including maintenance of quiescence, proliferation, and differentiation. The article specifically focuses on the role of histone modifications and DNA methylation in quiescent stem cells, and how these modifications can be dynamically regulated by environmental cues. The future perspectives of quiescent stem cell research are also discussed, including their potential for tissue repair and regeneration, their role in aging and age-related diseases, and their implications for cancer research. Overall, this review provides a comprehensive overview of the epigenetic regulation of quiescent stem cells and highlights the potential of this research for the development of new therapies in regenerative medicine, aging research, and cancer biology.

Keywords

epigenetic regulation - quiescent stem cells - histone modifications - DNA methylation - molecular signature - environmental cues - tissue repair

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Referenzen

References
1 Chowdhury S, Ghosh S, Chowdhury S, Ghosh S. Stem cells an overview. Stem cells. Biol Ther 2021; 1-21
2 Stripp BR, Reynolds SD. Maintenance and repair of the bronchiolar epithelium. Proc Am Thorac Soc 2008; 5 (03) 328-333
3 van Velthoven CTJ, Rando TA. Stem cell quiescence: dynamism, restraint, and cellular idling. Cell Stem Cell 2019; 24 (02) 213-225
4 de Morree A, Rando TA. Regulation of adult stem cell quiescence and its functions in the maintenance of tissue integrity. Nat Rev Mol Cell Biol 2023; 24 (05) 334-354
5 Goodell MA, Nguyen H, Shroyer N. Somatic stem cell heterogeneity: diversity in the blood, skin and intestinal stem cell compartments. Nat Rev Mol Cell Biol 2015; 16 (05) 299-309
6 Marqués-Torrejón MÁ, Williams CAC, Southgate B. et al. LRIG1 is a gatekeeper to exit from quiescence in adult neural stem cells. Nat Commun 2021; 12 (01) 2594
7 Arai F, Suda T. Maintenance of quiescent hematopoietic stem cells in the osteoblastic niche. Ann N Y Acad Sci 2007; 1106 (01) 41-53
8 Vitale I, Manic G, De Maria R, Kroemer G, Galluzzi L. DNA damage in stem cells. Mol Cell 2017; 66 (03) 306-319
9 Tümpel S, Rudolph KL. Quiescence: good and bad of stem cell aging. Trends Cell Biol 2019; 29 (08) 672-685
10 Trentesaux C, Striedinger K, Pomerantz JH, Klein OD. From gut to glutes: the critical role of niche signals in the maintenance and renewal of adult stem cells. Curr Opin Cell Biol 2020; 63: 88-101
11 Morizur L, Chicheportiche A, Gauthier LR, Daynac M, Boussin FD, Mouthon M-A. Distinct molecular signatures of quiescent and activated adult neural stem cells reveal specific interactions with their microenvironment. Stem Cell Reports 2018; 11 (02) 565-577
12 Cheung TH, Rando TA. Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 2013; 14 (06) 329-340
13 Lee SA, Li KN, Tumbar T. Stem cell-intrinsic mechanisms regulating adult hair follicle homeostasis. Exp Dermatol 2021; 30 (04) 430-447
14 Beerman I, Seita J, Inlay MA, Weissman IL, Rossi DJ. Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell 2014; 15 (01) 37-50
15 Ermolaeva M, Neri F, Ori A, Rudolph KL. Cellular and epigenetic drivers of stem cell ageing. Nat Rev Mol Cell Biol 2018; 19 (09) 594-610
16 Nakhaei-Rad S, Nakhaeizadeh H, Götze S. et al. The role of embryonic stem cell-expressed RAS (ERAS) in the maintenance of quiescent hepatic stellate cells. J Biol Chem 2016; 291 (16) 8399-8413
17 Mandal PK, Blanpain C, Rossi DJ. DNA damage response in adult stem cells: pathways and consequences. Nat Rev Mol Cell Biol 2011; 12 (03) 198-202
18 Liu L, Cheung TH, Charville GW. et al. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep 2013; 4 (01) 189-204
19 Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology 2013; 38 (01) 23-38
20 Chen Z, Guo Q, Song G, Hou Y. Molecular regulation of hematopoietic stem cell quiescence. Cell Mol Life Sci 2022; 79 (04) 218
21 Karimian A, Ahmadi Y, Yousefi B. Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Repair (Amst) 2016; 42: 63-71
22 Pepenella S, Murphy KJ, Hayes JJ. Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure. Chromosoma 2014; 123 (1-2): 3-13
23 Martynoga B, Mateo JL, Zhou B. et al. Epigenomic enhancer annotation reveals a key role for NFIX in neural stem cell quiescence. Genes Dev 2013; 27 (16) 1769-1786
24 Yang J, Tang Y, Liu H, Guo F, Ni J, Le W. Suppression of histone deacetylation promotes the differentiation of human pluripotent stem cells towards neural progenitor cells. BMC Biol 2014; 12: 95
25 Wu H, Sun YE. Epigenetic regulation of stem cell differentiation. Pediatr Res 2006; 59 (4 Pt 2): 21R-25R
26 Frye M, Fisher AG, Watt FM. Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS One 2007; 2 (08) e763
27 Luo M, Li J-F, Yang Q. et al. Stem cell quiescence and its clinical relevance. World J Stem Cells 2020; 12 (11) 1307-1326
28 Yang Y, Kueh AJ, Grant ZL. et al. The histone lysine acetyltransferase HBO1 (KAT7) regulates hematopoietic stem cell quiescence and self-renewal. Blood 2022; 139 (06) 845-858
29 Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 2004; 101 (47) 16659-16664
30 Yang Z, Shah K, Khodadadi-Jamayran A, Jiang H. Control of hematopoietic stem and progenitor cell function through epigenetic regulation of energy metabolism and genome integrity. Stem Cell Reports 2019; 13 (01) 61-75
31 Murao N, Noguchi H, Nakashima K. Epigenetic regulation of neural stem cell property from embryo to adult. Neuroepigenetics 2016; 5: 1-10
32 Fagnocchi L, Mazzoleni S, Zippo A. Integration of signaling pathways with the epigenetic machinery in the maintenance of stem cells. Stem Cells Int 2016; 2016: 8652748
33 Klemm SL, Shipony Z, Greenleaf WJ. Chromatin accessibility and the regulatory epigenome. Nat Rev Genet 2019; 20 (04) 207-220
34 Sun S, Jiang N, Jiang Y. et al. Chromatin remodeler Znhit1 preserves hematopoietic stem cell quiescence by determining the accessibility of distal enhancers. Leukemia 2020; 34 (12) 3348-3358
35 Tu Z, Zheng Y. Role of ATP-dependent chromatin remodelers in hematopoietic stem and progenitor cell maintenance. Curr Opin Hematol 2022; 29 (04) 174-180
36 Krasteva V, Crabtree GR, Lessard JA. The BAF45a/PHF10 subunit of SWI/SNF-like chromatin remodeling complexes is essential for hematopoietic stem cell maintenance. Exp Hematol 2017; 48: 58-71.e15
37 Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML. Transcription factor YY1 functions as a PcG protein in vivo. EMBO J 2003; 22 (06) 1347-1358
38 Lu Z, Hong CC, Kong G. et al. Polycomb group protein YY1 is an essential regulator of hematopoietic stem cell quiescence. Cell Rep 2018; 22 (06) 1545-1559
39 Bode D, Yu L, Tate P, Pardo M, Choudhary J. Characterization of two distinct nucleosome remodeling and deacetylase (NuRD) complex assemblies in embryonic stem cells. Mol Cell Proteomics 2016; 15 (03) 878-891
40 Angeloni A, Bogdanovic O. Enhancer DNA methylation: implications for gene regulation. Essays Biochem 2019; 63 (06) 707-715
41 Miller JL, Grant PA. The role of DNA methylation and histone modifications in transcriptional regulation in humans. Subcell Biochem 2013; 61: 289-317
42 Momparler RL, Côté S, Momparler LF. Epigenetic modulation of self-renewal capacity of leukemic stem cells and implications for chemotherapy. Epigenomes 2020; 4 (01) 3
43 Cheng Y, Xie N, Jin P, Wang T. DNA methylation and hydroxymethylation in stem cells. Cell Biochem Funct 2015; 33 (04) 161-173
44 Ancel S, Stuelsatz P, Feige JN. Muscle stem cell quiescence: controlling stemness by staying asleep. Trends Cell Biol 2021; 31 (07) 556-568
45 Breton-Larrivée M, Elder E, McGraw S. DNA methylation, environmental exposures and early embryo development. Anim Reprod 2019; 16 (03) 465-474