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Volume 49 Issue 4
Apr.  2022
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Article Contents

Epigenome-Metabolome-Epigenome signaling cascade in cell biological processes

doi: 10.1016/j.jgg.2021.09.006
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We are grateful to all members in Professor Xingguo Liu's laboratory for useful discussions. This work was financially supported by the National Key Research and Development Program of China (2017YFA0106300), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA16030505), the National Natural Science Foundation projects of China (2017YFA0102900, 2019YFA09004500, 2017YFC1001602, 2016YFA0100300, 2018YFA0107100), the National Natural Science Foundation projects of China (92157202, 32025010, 31801168, 31900614, 31970709, 81901275, 32070729, 32100619, 32170747), the Key Research Program of Frontier Sciences, CAS (QYZDB-SSW-SMC001), and International Cooperation Program (154144KYSB20200006), Guangdong Province Science and Technology Program (2020B1212060052, 2018A030313825, 2018GZR110103002, 2020A1515011200, 2020A1515010919, 2020A1515011410, 2021A1515012513), Guangzhou Science and Technology Program (201807010067, 202002030277, 202102021250, 202102020827, 202102080066), Open Research Program of Key Laboratory of Regenerative Biology, CAS (KLRB201907, KLRB202014), and CAS Youth Innovation Promotion Association (to Y. W. and K. C.).

  • Received Date: 2021-06-04
  • Accepted Date: 2021-09-01
  • Rev Recd Date: 2021-09-01
  • Publish Date: 2022-04-30
  • Cell fate determination as a fundamental question in cell biology has been extensively studied at different regulatory levels for many years. However, the mechanisms of multilevel regulation of cell fate determination remain unclear. Recently, we have proposed an Epigenome-Metabolome-Epigenome (E-M-E) signaling cascade model to describe the cross-over cooperation during mouse somatic cell reprogramming. In this review, we summarize the broad roles of E-M-E signaling cascade in different cell biological processes, including cell differentiation and dedifferentiation, cell specialization, cell proliferation, and cell pathologic processes. Precise E-M-E signaling cascades are critical in these cell biological processes, and it is of worth to explore each step of E-M-E signaling cascade. E-M-E signaling cascade model sheds light on and may open a window to explore the mechanisms of multilevel regulation of cell biological processes.
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  • Aune, T.M., Collins, P.L.,Chang, S., 2009. Epigenetics and T helper 1 differentiation. Immunology 126, 299-305
    Bulusu, V.,Aulehla, A., 2016. Metabolic Control of Cellular Differentiation. Dev. Cell 39, 286-287
    Cai, L., Sutter, B.M., Li, B.,Tu, B.P., 2011. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 42, 426-437
    Cao, Y., Guo, W.T., Tian, S., He, X., Wang, X.W., Liu, X., Gu, K.L., Ma, X., Huang, D., Hu, L., et al., 2015. miR-290/371-Mbd2-Myc circuit regulates glycolytic metabolism to promote pluripotency. EMBO J. 34, 609-623
    Cao, S., Yu, S., Li, D., Ye, J., Yang, X., Li, C., Wang, X., Mai, Y., Qin, Y., Wu, J., et al., 2018. Chromatin Accessibility Dynamics during Chemical Induction of Pluripotency. Cell Stem Cell 22, 529-542 e525
    Carey, B.W., Finley, L.W., Cross, J.R., Allis, C.D.,Thompson, C.B., 2015. Intracellular alpha-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 518, 413-416
    Casey, M.J., Stumpf, P.S.,MacArthur, B.D., 2020. Theory of cell fate. Wiley interdiscip. Rev. Syst. Bio. Med. 12, e1471
    Cha, Y., Han, M.J., Cha, H.J., Zoldan, J., Burkart, A., Jung, J.H., Jang, Y., Kim, C.H., Jeong, H.C., Kim, B.G., et al., 2017. Metabolic control of primed human pluripotent stem cell fate and function by the miR-200c-SIRT2 axis. Nat. Cell Biol. 19, 445-456
    Chen, J., Liu, H., Liu, J., Qi, J., Wei, B., Yang, J., Liang, H., Chen, Y., Chen, J., Wu, Y., et al., 2013a. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat.Genet. 45, 34-42
    Chen, Q., Chen, Y., Bian, C., Fujiki, R.,Yu, X., 2013b. TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 493, 561-564
    Chen, K., Long, Q., Xing, G., Wang, T., Wu, Y., Li, L., Qi, J., Zhou, Y., Ma, B., Scholer, H.R., et al., 2019. Heterochromatin loosening by the Oct4 linker region facilitates Klf4 binding and iPSC reprogramming. EMBO J. e99165
    Chu, Y., Jiang, M., Wu, N., Xu, B., Li, W., Liu, H., Su, S., Shi, Y., Liu, H., Gao, X., et al., 2020. O-GlcNAcylation of SIX1 enhances its stability and promotes Hepatocellular Carcinoma Proliferation. Theranostics 10, 9830-9842
    Cliff, T.S., Wu, T., Boward, B.R., Yin, A., Yin, H., Glushka, J.N., Prestegaard, J.H.,Dalton, S., 2017. MYC Controls Human Pluripotent Stem Cell Fate Decisions through Regulation of Metabolic Flux. Cell Stem Cell 21, 502-516.e509
    Dang, C.V., Le, A.,Gao, P., 2009. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin. Cancer Res. 15, 6479-6483
    de Boer, V.C.,Houten, S.M., 2014. A mitochondrial expatriate: nuclear pyruvate dehydrogenase. Cell 158, 9-10
    Fang, Y., Xu, X., Ding, J., Yang, L., Doan, M.T., Karmaus, P.W.F., Snyder, N.W., Zhao, Y., Li, J.L.,Li, X., 2021. Histone crotonylation promotes mesoendodermal commitment of human embryonic stem cells. Cell Stem Cell 28, 748-763 e747
    Fernandez-Rebollo, E., Franzen, J., Goetzke, R., Hollmann, J., Ostrowska, A., Oliverio, M., Sieben, T., Rath, B., Kornfeld, J.W.,Wagner, W., 2020. Senescence-Associated Metabolomic Phenotype in Primary and iPSC-Derived Mesenchymal Stromal Cells. Stem Cell Reports 14, 201-209
    Folmes, C.D., Nelson, T.J., Martinez-Fernandez, A., Arrell, D.K., Lindor, J.Z., Dzeja, P.P., Ikeda, Y., Perez-Terzic, C.,Terzic, A., 2011. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab. 14, 264-271
    Fu, X., Wu, X., Djekidel, M.N.,Zhang, Y., 2019. Myc and Dnmt1 impede the pluripotent to totipotent state transition in embryonic stem cells. Nat. Cell Biol. 21, 835-844
    Gorgoulis, V., Adams, P.D., Alimonti, A., Bennett, D.C., Bischof, O., Bishop, C., Campisi, J., Collado, M., Evangelou, K., Ferbeyre, G., et al., 2019. Cellular Senescence: Defining a Path Forward. Cell 179, 813-827
    Gurdon, J.B., 1962. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol Exp. Morphol. 10, 622-640
    Gurdon, J.B., 2013. The cloning of a frog. Development 140, 2446-2448
    Hanover, J.A., 2010. Epigenetics gets sweeter: O-GlcNAc joins the "histone code". Chem. Biol. 17, 1272-1274
    Hoefflin, R., Harlander, S., Schafer, S., Metzger, P., Kuo, F., Schonenberger, D., Adlesic, M., Peighambari, A., Seidel, P., Chen, C.Y., et al., 2020. HIF-1alpha and HIF-2alpha differently regulate tumour development and inflammation of clear cell renal cell carcinoma in mice. Nat. Commun.11, 4111
    Hu, S., Balakrishnan, A., Bok, R.A., Anderton, B., Larson, P.E., Nelson, S.J., Kurhanewicz, J., Vigneron, D.B.,Goga, A., 2011. 13C-pyruvate imaging reveals alterations in glycolysis that precede c-Myc-induced tumor formation and regression. Cell Metab. 14, 131-142
    Hu, Z., Tan, D.E.K., Chia, G., Tan, H., Leong, H.F., Chen, B.J., Lau, M.S., Tan, K.Y.S., Bi, X., Yang, D., et al., 2020. Maternal factor NELFA drives a 2C-like state in mouse embryonic stem cells. Nat. Cell Biol. 22, 175-186
    Hwang, I.Y., Kwak, S., Lee, S., Kim, H., Lee, S.E., Kim, J.H., Kim, Y.A., Jeon, Y.K., Chung, D.H., Jin, X., et al., 2016. Psat1-Dependent Fluctuations in alpha-Ketoglutarate Affect the Timing of ESC Differentiation. Cell Metab. 24, 494-501
    Intlekofer, A.M.,Finley, L.W.S., 2019. Metabolic signatures of cancer cells and stem cells. Nat. Metab. 1, 177-188
    Jang, H., Kim, T.W., Yoon, S., Choi, S.Y., Kang, T.W., Kim, S.Y., Kwon, Y.W., Cho, E.J.,Youn, H.D., 2012. O-GlcNAc regulates pluripotency and reprogramming by directly acting on core components of the pluripotency network. Cell Stem Cell 11, 62-74
    Jones, P.A., Issa, J.P.,Baylin, S., 2016. Targeting the cancer epigenome for therapy. Nat. Rev. Genet. 17, 630-641
    Khaw, S.L., Min-Wen, C., Koh, C.G., Lim, B.,Shyh-Chang, N., 2015. Oocyte Factors Suppress Mitochondrial Polynucleotide Phosphorylase to Remodel the Metabolome and Enhance Reprogramming. Cell Rep. 12, 1080-1088
    Kim, H., Jang, H., Kim, T.W., Kang, B.H., Lee, S.E., Jeon, Y.K., Chung, D.H., Choi, J., Shin, J., Cho, E.J., et al., 2015. Core Pluripotency Factors Directly Regulate Metabolism in Embryonic Stem Cell to Maintain Pluripotency. Stem Cells 33, 2699-2711
    Le, R., Huang, Y., Zhao, A.,Gao, S., 2020. Lessons from expanded potential of embryonic stem cells: Moving toward totipotency. J. Genet. Genomics 47, 123-130
    Lee, J.V., Carrer, A., Shah, S., Snyder, N.W., Wei, S., Venneti, S., Worth, A.J., Yuan, Z.F., Lim, H.W., Liu, S., et al., 2014. Akt-dependent metabolic reprogramming regulates tumor cell histone acetylation. Cell Metab. 20, 306-319
    Letouze, E., Martinelli, C., Loriot, C., Burnichon, N., Abermil, N., Ottolenghi, C., Janin, M., Menara, M., Nguyen, A.T., Benit, P., et al., 2013. SDH mutations establish a hypermethylator phenotype in paraganglioma. Cancer Cell 23, 739-752
    Lewis, B.A.,Hanover, J.A., 2014. O-GlcNAc and the epigenetic regulation of gene expression. J. Biol. Chem. 289, 34440-34448
    Li, R., Liang, J., Ni, S., Zhou, T., Qing, X., Li, H., He, W., Chen, J., Li, F., Zhuang, Q., et al., 2010. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7, 51-63
    Li, D., Liu, J., Yang, X., Zhou, C., Guo, J., Wu, C., Qin, Y., Guo, L., He, J., Yu, S., et al., 2017. Chromatin Accessibility Dynamics during iPSC Reprogramming. Cell Stem Cell 21, 819-833 e816
    Li, L., Liang, Y., Kang, L., Liu, Y., Gao, S., Chen, S., Li, Y., You, W., Dong, Q., Hong, T., et al., 2018. Transcriptional Regulation of the Warburg Effect in Cancer by SIX1. Cancer Cell 33, 368-385 e367
    Li, L., Chen, K., Wang, T., Wu, Y., Xing, G., Chen, M., Hao, Z., Zhang, C., Zhang, J., Ma, B., et al., 2020. Glis1 facilitates induction of pluripotency via an epigenome-metabolome-epigenome signalling cascade. Nat. Metab. 2, 882-892
    Liu, X., Sun, H., Qi, J., Wang, L., He, S., Liu, J., Feng, C., Chen, C., Li, W., Guo, Y., et al., 2013. Sequential introduction of reprogramming factors reveals a time-sensitive requirement for individual factors and a sequential EMT-MET mechanism for optimal reprogramming. Nat. Cell Biol. 15, 829-838
    Liu, L., Xu, Y., He, M., Zhang, M., Cui, F., Lu, L., Yao, M., Tian, W., Benda, C., Zhuang, Q., et al., 2014. Transcriptional pause release is a rate-limiting step for somatic cell reprogramming. Cell Stem Cell 15, 574-588
    Ma, X., Li, C., Sun, L., Huang, D., Li, T., He, X., Wu, G., Yang, Z., Zhong, X., Song, L., et al., 2014. Lin28/let-7 axis regulates aerobic glycolysis and cancer progression via PDK1. Nat. Commun. 5, 5212
    Mathieu, J., Zhou, W., Xing, Y., Sperber, H., Ferreccio, A., Agoston, Z., Kuppusamy, K.T., Moon, R.T.,Ruohola-Baker, H., 2014. Hypoxia-inducible factors have distinct and stage-specific roles during reprogramming of human cells to pluripotency. Cell Stem Cell 14, 592-605
    Mayor, R., 2019. Cell fate decisions during development. Science 364, 937-938
    Mews, P., Donahue, G., Drake, A.M., Luczak, V., Abel, T.,Berger, S.L., 2017. Acetyl-CoA synthetase regulates histone acetylation and hippocampal memory. Nature 546, 381-386
    Miranda-Goncalves, V., Lameirinhas, A., Henrique, R.,Jeronimo, C., 2018. Metabolism and Epigenetic Interplay in Cancer: Regulation and Putative Therapeutic Targets. Front. Genet. 9, 427
    Monk, D., Mackay, D.J.G., Eggermann, T., Maher, E.R.,Riccio, A., 2019. Genomic imprinting disorders: lessons on how genome, epigenome and environment interact. Nat. Rev. Genet. 20, 235-248
    Moris, N., Pina, C.,Arias, A.M., 2016. Transition states and cell fate decisions in epigenetic landscapes. Nat. Rev. Genet. 17, 693-703
    Morris, J.P.t., Yashinskie, J.J., Koche, R., Chandwani, R., Tian, S., Chen, C.C., Baslan, T., Marinkovic, Z.S., Sanchez-Rivera, F.J., Leach, S.D., et al., 2019. alpha-Ketoglutarate links p53 to cell fate during tumour suppression. Nature 573, 595-599
    Moussaieff, A., Rouleau, M., Kitsberg, D., Cohen, M., Levy, G., Barasch, D., Nemirovski, A., Shen-Orr, S., Laevsky, I., Amit, M., et al., 2015. Glycolysis-mediated changes in acetyl-CoA and histone acetylation control the early differentiation of embryonic stem cells. Cell Metab. 21, 392-402
    Nacarelli, T.,Sell, C., 2017. Targeting metabolism in cellular senescence, a role for intervention. Mol. Cell. Endocrinol. 455, 83-92
    Nagaraj, R., Sharpley, M.S., Chi, F., Braas, D., Zhou, Y., Kim, R., Clark, A.T.,Banerjee, U., 2017. Nuclear Localization of Mitochondrial TCA Cycle Enzymes as a Critical Step in Mammalian Zygotic Genome Activation. Cell 168, 210-223 e211
    Papait, R., Serio, S.,Condorelli, G., 2020. Role of the Epigenome in Heart Failure. Physiol. Rev. 100, 1753-1777
    Pavlova, N.N.,Thompson, C.B., 2016. The Emerging Hallmarks of Cancer Metabolism. Cell Metab. 23, 27-47
    Pei, D., Shu, X., Gassama-Diagne, A.,Thiery, J.P., 2019. Mesenchymal-epithelial transition in development and reprogramming. Nat. Cell Biol. 21, 44-53
    Peng, M., Yin, N., Chhangawala, S., Xu, K., Leslie, C.S.,Li, M.O., 2016. Aerobic glycolysis promotes T helper 1 cell differentiation through an epigenetic mechanism. Science 354, 481-484
    Polo, J.M., Anderssen, E., Walsh, R.M., Schwarz, B.A., Nefzger, C.M., Lim, S.M., Borkent, M., Apostolou, E., Alaei, S., Cloutier, J., et al., 2012. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151, 1617-1632
    Rodriguez-Terrones, D., Hartleben, G., Gaume, X., Eid, A., Guthmann, M., Iturbide, A.,Torres-Padilla, M.E., 2020. A distinct metabolic state arises during the emergence of 2-cell-like cells. EMBO Rep. 21, e48354
    Sakabe, K., Wang, Z.,Hart, G.W., 2010. Beta-N-acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl. Acad. Sci. U. S. A. 107, 19915-19920
    Sardina, J.L., Collombet, S., Tian, T.V., Gomez, A., Di Stefano, B., Berenguer, C., Brumbaugh, J., Stadhouders, R., Segura-Morales, C., Gut, M., et al., 2018. Transcription Factors Drive Tet2-Mediated Enhancer Demethylation to Reprogram Cell Fate. Cell Stem Cell 23, 727-741 e729
    Sebastian, C., Zwaans, B.M., Silberman, D.M., Gymrek, M., Goren, A., Zhong, L., Ram, O., Truelove, J., Guimaraes, A.R., Toiber, D., et al., 2012. The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism. Cell 151, 1185-1199
    Shiraki, N., Shiraki, Y., Tsuyama, T., Obata, F., Miura, M., Nagae, G., Aburatani, H., Kume, K., Endo, F.,Kume, S., 2014. Methionine metabolism regulates maintenance and differentiation of human pluripotent stem cells. Cell Metab. 19, 780-794
    Shyh-Chang, N., Locasale, J.W., Lyssiotis, C.A., Zheng, Y., Teo, R.Y., Ratanasirintrawoot, S., Zhang, J., Onder, T., Unternaehrer, J.J., Zhu, H., et al., 2013. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 339, 222-226
    Sone, M., Morone, N., Nakamura, T., Tanaka, A., Okita, K., Woltjen, K., Nakagawa, M., Heuser, J.E., Yamada, Y., Yamanaka, S., et al., 2017. Hybrid Cellular Metabolism Coordinated by Zic3 and Esrrb Synergistically Enhances Induction of Naive Pluripotency. Cell Metab. 25, 1103-1117 e1106
    Speakman, C.M., Domke, T.C., Wongpaiboonwattana, W., Sanders, K., Mudaliar, M., van Aalten, D.M., Barton, G.J.,Stavridis, M.P., 2014. Elevated O-GlcNAc levels activate epigenetically repressed genes and delay mouse ESC differentiation without affecting naive to primed cell transition. Stem Cells 32, 2605-2615
    Sutendra, G., Kinnaird, A., Dromparis, P., Paulin, R., Stenson, T.H., Haromy, A., Hashimoto, K., Zhang, N., Flaim, E.,Michelakis, E.D., 2014. A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 158, 84-97
    Takahashi, K.,Yamanaka, S., 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676
    Takahashi, K.,Yamanaka, S., 2016. A decade of transcription factor-mediated reprogramming to pluripotency. Nature reviews Mol. Cell Biol. 17, 183-193
    Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K.,Yamanaka, S., 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872
    Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Sasaki, A., Yamamoto, M., Nakamura, M., Sutou, K., Osafune, K.,Yamanaka, S., 2014. Induction of pluripotency in human somatic cells via a transient state resembling primitive streak-like mesendoderm. Nat. Commun. 5, 3678
    Shin-ichiro Takebayashi, Hiroshi Tanaka, Shinjiro Hino, Yuko Nakatsu, Tomoka Igata, Akihisa Sakamoto,Nakao, M.N.a.M., 2015. Retinoblastoma protein promotes oxidative phosphorylation. Aging Cell 14, 689-697
    Tatapudy, S., Aloisio, F., Barber, D.,Nystul, T., 2017. Cell fate decisions: emerging roles for metabolic signals and cell morphology. EMBO Rep. 18, 2105-2118
    TeSlaa, T., Chaikovsky, A.C., Lipchina, I., Escobar, S.L., Hochedlinger, K., Huang, J., Graeber, T.G., Braas, D.,Teitell, M.A., 2016. alpha-Ketoglutarate Accelerates the Initial Differentiation of Primed Human Pluripotent Stem Cells. Cell Metab. 24, 485-493
    Thakur, C.,Chen, F., 2019. Connections between metabolism and epigenetics in cancers. Semin. Cancer Biol. 57, 52-58
    Vella, P., Scelfo, A., Jammula, S., Chiacchiera, F., Williams, K., Cuomo, A., Roberto, A., Christensen, J., Bonaldi, T., Helin, K., et al., 2013. Tet proteins connect the O-linked N-acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol. Cell 49, 645-656
    Wan, W., Peng, K., Li, M., Qin, L., Tong, Z., Yan, J., Shen, B.,Yu, C., 2017. Histone demethylase JMJD1A promotes urinary bladder cancer progression by enhancing glycolysis through coactivation of hypoxia inducible factor 1alpha. Oncogene 36, 3868-3877
    Wang, J., Alexander, P., Wu, L., Hammer, R., Cleaver, O.,McKnight, S.L., 2009. Dependence of mouse embryonic stem cells on threonine catabolism. Science 325, 435-439
    Wang, L., Zhang, T., Wang, L., Cai, Y., Zhong, X., He, X., Hu, L., Tian, S., Wu, M., Hui, L., et al., 2017. Fatty acid synthesis is critical for stem cell pluripotency via promoting mitochondrial fission. EMBO J. 36, 1330-1347
    Wiley, C.D.,Campisi, J., 2016. From Ancient Pathways to Aging Cells-Connecting Metabolism and Cellular Senescence. Cell Metab. 23, 1013-1021
    Wilson, C.B., Rowell, E.,Sekimata, M., 2009. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 9, 91-105
    Wong, B.W., Wang, X., Zecchin, A., Thienpont, B., Cornelissen, I., Kalucka, J., Garcia-Caballero, M., Missiaen, R., Huang, H., Bruning, U., et al., 2017a. The role of fatty acid beta-oxidation in lymphangiogenesis. Nature 542, 49-54
    Wong, C.C., Qian, Y.,Yu, J., 2017b. Interplay between epigenetics and metabolism in oncogenesis: mechanisms and therapeutic approaches. Oncogene 36, 3359-3374
    Wu, D., Cai, Y.,Jin, J., 2017. Potential coordination role between O-GlcNAcylation and epigenetics. Protein Cell 8, 713-723
    Wu, Y., Chen, K., Liu, X., Huang, L., Zhao, D., Li, L., Gao, M., Pei, D., Wang, C.,Liu, X., 2016. Srebp-1 Interacts with c-Myc to Enhance Somatic Cell Reprogramming. Stem Cells 34, 83-92
    Wu, Y., Chen, K., Xing, G., Li, L., Ma, B., Hu, Z., Duan, L.,Liu, X., 2019. Phospholipid remodeling is critical for stem cell pluripotency by facilitating mesenchymal-to-epithelial transition. Sci. Adv. 5, eaax7525
    Xie, Y., Jin, P., Sun, X., Jiao, T., Zhang, Y., Li, Y.,Sun, M., 2018. SIX1 is upregulated in gastric cancer and regulates proliferation and invasion by targeting the ERK pathway and promoting epithelial-mesenchymal transition. Cell Biochem. Funct. 36, 413-419
    Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.H., Ito, S., Yang, C., Wang, P., Xiao, M.T., et al., 2011. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19, 17-30
    Xu, Y., Zhang, Y., Garcia-Canaveras, J.C., Guo, L., Kan, M., Yu, S., Blair, I.A., Rabinowitz, J.D.,Yang, X., 2020. Chaperone-mediated autophagy regulates the pluripotency of embryonic stem cells. Science 369, 397-403
    Yamanaka, S., 2012. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10, 678-684
    Yang, X.,Qian, K., 2017. Protein O-GlcNAcylation: emerging mechanisms and functions. Nat. Rev. Mol. Cell Biol. 18, 452-465
    Yang, X., Zhao, H., Yang, J., Ma, Y., Liu, Z., Li, C., Wang, T., Yan, Z.,Du, N., 2019. MiR-150-5p regulates melanoma proliferation, invasion and metastasis via SIX1-mediated Warburg Effect. Biochem. Biophys. Res. Commun. 515, 85-91
    Ying, Z., Chen, K., Zheng, L., Wu, Y., Li, L., Wang, R., Long, Q., Yang, L., Guo, J., Yao, D., et al., 2016. Transient Activation of Mitoflashes Modulates Nanog at the Early Phase of Somatic Cell Reprogramming. Cell Metab. 23, 220-226
    Zechner, C., Nerli, E., Norden, C., 2020. Stochasticity and determinism in cell fate decisions. Development 147, dev181495
    Zhang, J., Nuebel, E., Daley, G.Q., Koehler, C.M.,Teitell, M.A., 2012. Metabolic regulation in pluripotent stem cells during reprogramming and self-renewal. Cell Stem Cell 11, 589-595
    Zhang, J., Ratanasirintrawoot, S., Chandrasekaran, S., Wu, Z., Ficarro, S.B., Yu, C., Ross, C.A., Cacchiarelli, D., Xia, Q., Seligson, M., et al., 2016. LIN28 Regulates Stem Cell Metabolism and Conversion to Primed Pluripotency. Cell Stem Cell 19, 66-80
    Zhao, Y., Zhao, T., Guan, J., Zhang, X., Fu, Y., Ye, J., Zhu, J., Meng, G., Ge, J., Yang, S., et al., 2015. A XEN-like State Bridges Somatic Cells to Pluripotency during Chemical Reprogramming. Cell 163, 1678-1691
    Zhu, Q., Cheng, X., Cheng, Y., Chen, J., Xu, H., Gao, Y., Duan, X., Ji, J., Li, X.,Yi, W., 2020. O-GlcNAcylation regulates the methionine cycle to promote pluripotency of stem cells. Proc.Natl. Acad. Sci. U. S. A. 117, 7755-7763
    Zhu, T., Zheng, J., Zhuo, W., Pan, P., Li, M., Zhang, W., Zhou, H., Gao, Y., Li, X.,Liu, Z., 2021. ETV4 promotes breast cancer cell stemness by activating glycolysis and CXCR4-mediated sonic Hedgehog signaling. Cell Death Discov. 7, 126
    Zhuang, Q., Li, W., Benda, C., Huang, Z., Ahmed, T., Liu, P., Guo, X., Ibanez, D.P., Luo, Z., Zhang, M., et al., 2018. NCoR/SMRT co-repressors cooperate with c-MYC to create an epigenetic barrier to somatic cell reprogramming. Nat. Cell Biol. 20, 400-412
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