Cellular metabolism and homeostasis in pluripotency regulation
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Protein & Cell
REVIEW Cellular metabolism and homeostasis in pluripotency regulation Kun Liu1,2,3, Jiani Cao1,2, Xingxing Shi1,2,3, Liang Wang1,2,3, Tongbiao Zhao1,2,3& State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 2 Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing 100101, China 3 University of Chinese Academy of Sciences, Beijing 100049, China & Correspondence: [email protected] (T. Zhao) Received September 14, 2019 Accepted June 18, 2020
ABSTRACT Pluripotent stem cells (PSCs) can immortally self-renew in culture with a high proliferation rate, and they possess unique metabolic characteristics that facilitate pluripotency regulation. Here, we review recent progress in understanding the mechanisms that link cellular metabolism and homeostasis to pluripotency regulation, with particular emphasis on pathways involving amino acid metabolism, lipid metabolism, the ubiquitin-proteasome system and autophagy. Metabolism of amino acids and lipids is tightly coupled to epigenetic modification, organelle remodeling and cell signaling pathways for pluripotency regulation. PSCs harness enhanced proteasome and autophagy activity to meet the material and energy requirements for cellular homeostasis. These regulatory events reflect a fine balance between the intrinsic cellular requirements and the extrinsic environment. A more complete understanding of this balance will pave new ways to manipulate PSC fate.
KEYWORDS autophagy, amino acid metabolism, lipid metabolism, pluripotent stem cell (PSC), ubiquitinproteasome system (UPS) INTRODUCTION Pluripotent stem cells (PSCs), including embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs), have the capacity to self-renew and differentiate into all cell types of our bodies (Liu et al., 2014; Martello and Smith,
Kun Liu, Jiani Cao and Xingxing Shi contributed equally.
© The Author(s) 2020
2014). These properties depend on a series of pluripotency genes that are highly expressed and coordinately regulated in PSCs (Boyer et al., 2005; Orkin and Hochedlinger, 2011). At the same time, PSCs have developed unique cell cycle characteristics and a high proliferation rate to match the activity of pluripotency gene networks (Wang et al., 2008; Singh and Dalton, 2009). Emerging evidence shows that metabolic pathways are mediators of crosstalk between cellular degradation, cellular recycling, epigenetic regulation, signal transduction and stem cell fate determination (Folmes et al., 2012; Buck et al., 2016; Gascon et al., 2016; Zhang et al., 2016b; Zheng et al., 2016). Cellular metabolism, including anabolism and catabolism, involves multiple complex biochemical processes, such as amino acid metabolism, nucleic acid metabolism, fatty acid metabolism, glycolysis, oxidative phosphorylation, the ubiquitin-proteasome degradation system, autophagy, and so on (Naujokat and Saric, 2007; Vessoni et al., 2012; Kilberg et al., 2016; Wang et al., 2017). Metabolism is not only
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