Molecules and Cells

  • 제46권12호
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  • Pages.727-735
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  • 2023
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  • 1016-8478(pISSN)
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  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
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Transcription Factor EB-Mediated Lysosomal Function Regulation for Determining Stem Cell Fate under Metabolic Stress

  • Chang Woo Chae (Department of Veterinary Physiology, College of Veterinary Medicine, Research Institute for Veterinary Science, and BK21 Four Future Veterinary Medicine Leading Education & Research Center, Seoul National University) ;
  • Young Hyun Jung (Department of Physiology, College of Medicine, Soonchunhyang University) ;
  • Ho Jae Han (Department of Veterinary Physiology, College of Veterinary Medicine, Research Institute for Veterinary Science, and BK21 Four Future Veterinary Medicine Leading Education & Research Center, Seoul National University)
  • 투고 : 2023.08.25
  • 심사 : 2023.10.20
  • 발행 : 2023.12.31
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초록

Stem cells require high amounts of energy to replicate their genome and organelles and differentiate into numerous cell types. Therefore, metabolic stress has a major impact on stem cell fate determination, including self-renewal, quiescence, and differentiation. Lysosomes are catabolic organelles that influence stem cell function and fate by regulating the degradation of intracellular components and maintaining cellular homeostasis in response to metabolic stress. Lysosomal functions altered by metabolic stress are tightly regulated by the transcription factor EB (TFEB) and TFE3, critical regulators of lysosomal gene expression. Therefore, understanding the regulatory mechanism of TFEB-mediated lysosomal function may provide some insight into stem cell fate determination under metabolic stress. In this review, we summarize the molecular mechanism of TFEB/TFE3 in modulating stem cell lysosomal function and then elucidate the role of TFEB/TFE3-mediated transcriptional activity in the determination of stem cell fate under metabolic stress.

키워드

과제정보

This research was supported by National R&D Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (RS-2023-00208475), and BK21 FOUR Future Veterinary Medicine Leading Education and Research Center.

참고문헌

  1. Annunziata, I., van de Vlekkert, D., Wolf, E., Finkelstein, D., Neale, G., Machado, E., Mosca, R., Campos, Y., Tillman, H., Roussel, M.F., et al. (2019). MYC competes with MiT/TFE in regulating lysosomal biogenesis and autophagy through an epigenetic rheostat. Nat. Commun. 10, 3623. 
  2. Ballabio, A. and Bonifacino, J.S. (2020). Lysosomes as dynamic regulators of cell and organismal homeostasis. Nat. Rev. Mol. Cell Biol. 21, 101-118.  https://doi.org/10.1038/s41580-019-0185-4
  3. Betschinger, J., Nichols, J., Dietmann, S., Corrin, P.D., Paddison, P.J., and Smith, A. (2013). Exit from pluripotency is gated by intracellular redistribution of the bHLH transcription factor Tfe3. Cell 153, 335-347.  https://doi.org/10.1016/j.cell.2013.03.012
  4. Borger, D.K., McMahon, B., Roshan Lal, T., Serra-Vinardell, J., Aflaki, E., and Sidransky, E. (2017). Induced pluripotent stem cell models of lysosomal storage disorders. Dis. Model. Mech. 10, 691-704.  https://doi.org/10.1242/dmm.029009
  5. Bradic, I., Liesinger, L., Kuentzel, K.B., Vujic, N., Trauner, M., Birner-Gruenberger, R., and Kratky, D. (2023). Metabolic changes and propensity for inflammation, fibrosis, and cancer in livers of mice lacking lysosomal acid lipase. J. Lipid Res. 64, 100427. 
  6. Chae, C.W., Choi, G.E., Jung, Y.H., Lim, J.R., Cho, J.H., Yoon, J.H., and Han, H.J. (2022). High glucose-mediated VPS26a down-regulation dysregulates neuronal amyloid precursor protein processing and tau phosphorylation. Br. J. Pharmacol. 179, 3934-3950.  https://doi.org/10.1111/bph.15836
  7. Chae, C.W., Lee, H.J., Choi, G.E., Jung, Y.H., Kim, J.S., Lim, J.R., Kim, S.Y., Hwang, I.K., Seong, J.K., and Han, H.J. (2020). High glucose-mediated PICALM and mTORC1 modulate processing of amyloid precursor protein via endosomal abnormalities. Br. J. Pharmacol. 177, 3828-3847.  https://doi.org/10.1111/bph.15131
  8. Chae, C.W., Yoon, J.H., Lim, J.R., Park, J.Y., Cho, J.H., Jung, Y.H., Choi, G.E., Lee, H.J., and Han, H.J. (2023). TRIM16-mediated lysophagy suppresses high-glucose-accumulated neuronal Aβ. Autophagy 19, 2752-2768.  https://doi.org/10.1080/15548627.2023.2229659
  9. Curnock, R., Yalci, K., Palmfeldt, J., Jaattela, M., Liu, B., and Carroll, B. (2023). TFEB-dependent lysosome biogenesis is required for senescence. EMBO J. 42, e111241. 
  10. de Almeida, M.J., Luchsinger, L.L., Corrigan, D.J., Williams, L.J., and Snoeck, H.W. (2017). Dye-independent methods reveal elevated mitochondrial mass in hematopoietic stem cells. Cell Stem Cell 21, 725-729.e4.  https://doi.org/10.1016/j.stem.2017.11.002
  11. Ferron, M., Settembre, C., Shimazu, J., Lacombe, J., Kato, S., Rawlings, D.J., Ballabio, A., and Karsenty, G. (2013). A RANKL-PKCβ-TFEB signaling cascade is necessary for lysosomal biogenesis in osteoclasts. Genes Dev. 27, 955-969.  https://doi.org/10.1101/gad.213827.113
  12. Furlan, G., Huyghe, A., Combemorel, N., and Lavial, F. (2023). Molecular versatility during pluripotency progression. Nat. Commun. 14, 68. 
  13. Garcia-Prat, L., Kaufmann, K.B., Schneiter, F., Voisin, V., Murison, A., Chen, J., Chan-Seng-Yue, M., Gan, O.I., McLeod, J.L., Smith, S.A., et al. (2021). TFEB-mediated endolysosomal activity controls human hematopoietic stem cell fate. Cell Stem Cell 28, 1838-1850.e10.  https://doi.org/10.1016/j.stem.2021.07.003
  14. Gollwitzer, P., Grutzmacher, N., Wilhelm, S., Kummel, D., and Demetriades, C. (2022). A Rag GTPase dimer code defines the regulation of mTORC1 by amino acids. Nat. Cell Biol. 24, 1394-1406.  https://doi.org/10.1038/s41556-022-00976-y
  15. Gros, F. and Muller, S. (2023). The role of lysosomes in metabolic and autoimmune diseases. Nat. Rev. Nephrol. 19, 366-383.  https://doi.org/10.1038/s41581-023-00692-2
  16. Halazonetis, T.D. and Kandil, A.N. (1991). Determination of the c-MYC DNA-binding site. Proc. Natl. Acad. Sci. U. S. A. 88, 6162-6166.  https://doi.org/10.1073/pnas.88.14.6162
  17. Hernandez-Segura, A., Nehme, J., and Demaria, M. (2018). Hallmarks of cellular senescence. Trends Cell Biol. 28, 436-453.  https://doi.org/10.1016/j.tcb.2018.02.001
  18. Hu, G., Xia, Y., Zhang, J., Chen, Y., Yuan, J., Niu, X., Zhao, B., Li, Q., Wang, Y., and Deng, Z. (2020a). ESC-sEVs rejuvenate senescent hippocampal NSCs by activating lysosomes to improve cognitive dysfunction in vascular dementia. Adv. Sci. (Weinh.) 7, 1903330. 
  19. Hu, Z., Li, H., Jiang, H., Ren, Y., Yu, X., Qiu, J., Stablewski, A.B., Zhang, B., Buck, M.J., and Feng, J. (2020b). Transient inhibition of mTOR in human pluripotent stem cells enables robust formation of mouse-human chimeric embryos. Sci. Adv. 6, eaaz0298. 
  20. Ito, K., Bonora, M., and Ito, K. (2019). Metabolism as master of hematopoietic stem cell fate. Int. J. Hematol. 109, 18-27.  https://doi.org/10.1007/s12185-018-2534-z
  21. Ito, K., Turcotte, R., Cui, J., Zimmerman, S.E., Pinho, S., Mizoguchi, T., Arai, F., Runnels, J.M., Alt, C., Teruya-Feldstein, J., et al. (2016). Self-renewal of a purified Tie2+ hematopoietic stem cell population relies on mitochondrial clearance. Science 354, 1156-1160.  https://doi.org/10.1126/science.aaf5530
  22. Jeon, J.H., Suh, H.N., Kim, M.O., Ryu, J.M., and Han, H.J. (2014). Glucosamine-induced OGT activation mediates glucose production through cleaved Notch1 and FoxO1, which coordinately contributed to the regulation of maintenance of self-renewal in mouse embryonic stem cells. Stem Cells Dev. 23, 2067-2079.  https://doi.org/10.1089/scd.2013.0583
  23. Jung, Y.H., Chae, C.W., Chang, H.S., Choi, G.E., Lee, H.J., and Han, H.J. (2022). Silencing SIRT5 induces the senescence of UCB-MSCs exposed to TNF-α by reduction of fatty acid β-oxidation and anti-oxidation. Free Radic. Biol. Med. 192, 1-12.  https://doi.org/10.1016/j.freeradbiomed.2022.09.002
  24. Kim, S., Song, H.S., Yu, J., and Kim, Y.M. (2021). MiT family transcriptional factors in immune cell functions. Mol. Cells 44, 342-355.  https://doi.org/10.14348/molcells.2021.0067
  25. Koh, Y.E., Choi, E.H., Kim, J.W., and Kim, K.P. (2022). The kleisin subunits of cohesin are involved in the fate determination of embryonic stem cells. Mol. Cells 45, 820-832.  https://doi.org/10.14348/molcells.2022.2042
  26. La Spina, M., Contreras, P.S., Rissone, A., Meena, N.K., Jeong, E., and Martina, J.A. (2021). MiT/TFE family of transcription factors: an evolutionary perspective. Front. Cell Dev. Biol. 8, 609683. 
  27. Lee, G. (2022). Cellular senescence: the villain of metabolic disease?: discovery of a distinct senescent cell population in obesity-induced metabolic dysfunction. Mol. Cells 45, 531-533.  https://doi.org/10.14348/molcells.2022.0084
  28. Lee, H.J., Jung, Y.H., Oh, J.Y., Choi, G.E., Chae, C.W., Kim, J.S., Lim, J.R., Kim, S.Y., Lee, S.J., Seong, J.K., et al. (2019). BICD1 mediates HIF1α nuclear translocation in mesenchymal stem cells during hypoxia adaptation. Cell Death Differ. 26, 1716-1734.  https://doi.org/10.1038/s41418-018-0241-1
  29. Li, Y., Xu, M., Ding, X., Yan, C., Song, Z., Chen, L., Huang, X., Wang, X., Jian, Y., Tang, G., et al. (2016). Protein kinase C controls lysosome biogenesis independently of mTORC1. Nat. Cell Biol. 18, 1065-1077.  https://doi.org/10.1038/ncb3407
  30. Liang, R., Arif, T., Kalmykova, S., Kasianov, A., Lin, M., Menon, V., Qiu, J., Bernitz, J.M., Moore, K., Lin, F., et al. (2020). Restraining lysosomal activity preserves hematopoietic stem cell quiescence and potency. Cell Stem Cell 26, 359-376.e7.  https://doi.org/10.1016/j.stem.2020.01.013
  31. Loeffler, D., Wehling, A., Schneiter, F., Zhang, Y., Muller-Botticher, N., Hoppe, P.S., Hilsenbeck, O., Kokkaliaris, K.D., Endele, M., and Schroeder, T. (2019). Asymmetric lysosome inheritance predicts activation of haematopoietic stem cells. Nature 573, 426-429.  https://doi.org/10.1038/s41586-019-1531-6
  32. Lopez-Otin, C., Blasco, M.A., Partridge, L., Serrano, M., and Kroemer, G. (2013). The hallmarks of aging. Cell 153, 1194-1217.  https://doi.org/10.1016/j.cell.2013.05.039
  33. Lu, H., Sun, J., Hamblin, M.H., Chen, Y.E., and Fan, Y. (2021). Transcription factor EB regulates cardiovascular homeostasis. EBioMedicine 63, 103207. 
  34. Mattes, K., Vellenga, E., and Schepers, H. (2019). Differential redox-regulation and mitochondrial dynamics in normal and leukemic hematopoietic stem cells: a potential window for leukemia therapy. Crit. Rev. Oncol. Hematol. 144, 102814. 
  35. Medina, D.L., Di Paola, S., Peluso, I., Armani, A., De Stefani, D., Venditti, R., Montefusco, S., Scotto-Rosato, A., Prezioso, C., Forrester, A., et al. (2015). Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat. Cell Biol. 17, 288-299.  https://doi.org/10.1038/ncb3114
  36. Murakami, K., Kurotaki, D., Kawase, W., Soma, S., Fukuchi, Y., Kunimoto, H., Yoshimi, R., Koide, S., Oshima, M., Hishiki, T., et al. (2021). OGT regulates hematopoietic stem cell maintenance via PINK1-dependent mitophagy. Cell Rep. 34, 108579. 
  37. Mutvei, A.P., Nagiec, M.J., Hamann, J.C., Kim, S.G., Vincent, C.T., and Blenis, J. (2020). Rap1-GTPases control mTORC1 activity by coordinating lysosome organization with amino acid availability. Nat. Commun. 11, 1416. 
  38. Palm, W. and Thompson, C.B. (2017). Nutrient acquisition strategies of mammalian cells. Nature 546, 234-242.  https://doi.org/10.1038/nature22379
  39. Pera, M.F. and Rossant, J. (2021). The exploration of pluripotency space: charting cell state transitions in peri-implantation development. Cell Stem Cell 28, 1896-1906.  https://doi.org/10.1016/j.stem.2021.10.001
  40. Raben, N. and Puertollano, R. (2016). TFEB and TFE3: linking lysosomes to cellular adaptation to stress. Annu. Rev. Cell Dev. Biol. 32, 255-278.  https://doi.org/10.1146/annurev-cellbio-111315-125407
  41. Ramazi, S. and Zahiri, J. (2021). Post-translational modifications in proteins: resources, tools and prediction methods. Database (Oxford) 2021, baab012. 
  42. Rossant, J. and Tam, P.P.L. (2022). Early human embryonic development: blastocyst formation to gastrulation. Dev. Cell 57, 152-165.  https://doi.org/10.1016/j.devcel.2021.12.022
  43. Samie, M. and Cresswell, P. (2015). The transcription factor TFEB acts as a molecular switch that regulates exogenous antigen-presentation pathways. Nat. Immunol. 16, 729-736.  https://doi.org/10.1038/ni.3196
  44. Settembre, C., Di Malta, C., Polito, V.A., Garcia Arencibia, M., Vetrini, F., Erdin, S., Erdin, S.U., Huynh, T., Medina, D., Colella, P., et al. (2011). TFEB links autophagy to lysosomal biogenesis. Science 332, 1429-1433.  https://doi.org/10.1126/science.1204592
  45. Sheng, Y., Ma, R., Yu, C., Wu, Q., Zhang, S., Paulsen, K., Zhang, J., Ni, H., Huang, Y., Zheng, Y., et al. (2021). Role of c-Myc haploinsufficiency in the maintenance of HSCs in mice. Blood 137, 610-623.  https://doi.org/10.1182/blood.2019004688
  46. Shyh-Chang, N. and Ng, H.H. (2017). The metabolic programming of stem cells. Genes Dev. 31, 336-346.  https://doi.org/10.1101/gad.293167.116
  47. Song, J.X., Sun, Y.R., Peluso, I., Zeng, Y., Yu, X., Lu, J.H., Xu, Z., Wang, M.Z., Liu, L.F., Huang, Y.Y., et al. (2016). A novel curcumin analog binds to and activates TFEB in vitro and in vivo independent of MTOR inhibition. Autophagy 12, 1372-1389.  https://doi.org/10.1080/15548627.2016.1179404
  48. Steingrimsson, E., Tessarollo, L., Pathak, B., Hou, L., Arnheiter, H., Copeland, N.G., and Jenkins, N.A. (2002). Mitf and Tfe3, two members of the Mitf-Tfe family of bHLH-Zip transcription factors, have important but functionally redundant roles in osteoclast development. Proc. Natl. Acad. Sci. U. S. A. 99, 4477-4482.  https://doi.org/10.1073/pnas.072071099
  49. Takihara, Y., Nakamura-Ishizu, A., Tan, D.Q., Fukuda, M., Matsumura, T., Endoh, M., Arima, Y., Chin, D.W.L., Umemoto, T., Hashimoto, M., et al. (2019). High mitochondrial mass is associated with reconstitution capacity and quiescence of hematopoietic stem cells. Blood Adv. 3, 2323-2327.  https://doi.org/10.1182/bloodadvances.2019032169
  50. Tan, A., Prasad, R., and Jho, E.H. (2021). TFEB regulates pluripotency transcriptional network in mouse embryonic stem cells independent of autophagy-lysosomal biogenesis. Cell Death Dis. 12, 343. 
  51. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., and Jones, J.M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.  https://doi.org/10.1126/science.282.5391.1145
  52. Vega-Rubin-de-Celis, S., Pena-Llopis, S., Konda, M., and Brugarolas, J. (2017). Multistep regulation of TFEB by MTORC1. Autophagy 13, 464-472.  https://doi.org/10.1080/15548627.2016.1271514
  53. Villegas, F., Lehalle, D., Mayer, D., Rittirsch, M., Stadler, M.B., Zinner, M., Olivieri, D., Vabres, P., Duplomb-Jego, L., De Bont, E., et al. (2019). Lysosomal signaling licenses embryonic stem cell differentiation via inactivation of Tfe3. Cell Stem Cell 24, 257-270.e8.  https://doi.org/10.1016/j.stem.2018.11.021
  54. Wang, H., Muthu Karuppan, M.K., Devadoss, D., Nair, M., Chand, H.S., and Lakshmana, M.K. (2021). TFEB protein expression is reduced in aged brains and its overexpression mitigates senescence-associated biomarkers and memory deficits in mice. Neurobiol. Aging 106, 26-36.  https://doi.org/10.1016/j.neurobiolaging.2021.06.003
  55. Wang, L., Han, X., Qu, G., Su, L., Zhao, B., and Miao, J. (2018). A pH probe inhibits senescence in mesenchymal stem cells. Stem Cell Res. Ther. 9, 343. 
  56. Williams, A.R. and Hare, J.M. (2011). Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ. Res. 109, 923-940.  https://doi.org/10.1161/CIRCRESAHA.111.243147
  57. Wilson, A., Murphy, M.J., Oskarsson, T., Kaloulis, K., Bettess, M.D., Oser, G.M., Pasche, A.C., Knabenhans, C., Macdonald, H.R., and Trumpp, A. (2004). c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 18, 2747-2763.  https://doi.org/10.1101/gad.313104
  58. Wolfson, R.L. and Sabatini, D.M. (2017). The dawn of the age of amino acid sensors for the mTORC1 pathway. Cell Metab. 26, 301-309.  https://doi.org/10.1016/j.cmet.2017.07.001
  59. Wunderlich, W., Fialka, I., Teis, D., Alpi, A., Pfeifer, A., Parton, R.G., Lottspeich, F., and Huber, L.A. (2001). A novel 14-kilodalton protein interacts with the mitogen-activated protein kinase scaffold mp1 on a late endosomal/lysosomal compartment. J. Cell Biol. 152, 765-776.  https://doi.org/10.1083/jcb.152.4.765
  60. Young, N.P., Kamireddy, A., Van Nostrand, J.L., Eichner, L.J., Shokhirev, M.N., Dayn, Y., and Shaw, R.J. (2016). AMPK governs lineage specification through Tfeb-dependent regulation of lysosomes. Genes Dev. 30, 535-552.  https://doi.org/10.1101/gad.274142.115
  61. Young, R.A. (2011). Control of the embryonic stem cell state. Cell 144, 940-954.  https://doi.org/10.1016/j.cell.2011.01.032
  62. Yun, S.P., Ryu, J.M., Park, J.H., Kim, M.O., Lee, J.H., and Han, H.J. (2012). Prostaglandin E2 maintains mouse ESC undifferentiated state through regulation of connexin31, connexin43 and connexin45 expression: involvement of glycogen synthase kinase 3β/β-catenin. Biol. Cell 104, 378-396.  https://doi.org/10.1111/boc.201100032
  63. Zhang, C.S., Jiang, B., Li, M., Zhu, M., Peng, Y., Zhang, Y.L., Wu, Y.Q., Li, T.Y., Liang, Y., Lu, Z., et al. (2014). The lysosomal v-ATPase-Ragulator complex is a common activator for AMPK and mTORC1, acting as a switch between catabolism and anabolism. Cell Metab. 20, 526-540.  https://doi.org/10.1016/j.cmet.2014.06.014
  64. Zhang, J., Wang, J., Zhou, Z., Park, J.E., Wang, L., Wu, S., Sun, X., Lu, L., Wang, T., Lin, Q., et al. (2018a). Importance of TFEB acetylation in control of its transcriptional activity and lysosomal function in response to histone deacetylase inhibitors. Autophagy 14, 1043-1059.  https://doi.org/10.1080/15548627.2018.1447290
  65. Zhang, J., Zhao, J., Dahan, P., Lu, V., Zhang, C., Li, H., and Teitell, M.A. (2018b). Metabolism in pluripotent stem cells and early mammalian development. Cell Metab. 27, 332-338.  https://doi.org/10.1016/j.cmet.2018.01.008
  66. Zhang, L., Pitcher, L.E., Prahalad, V., Niedernhofer, L.J., and Robbins, P.D. (2021). Recent advances in the discovery of senolytics. Mech. Ageing Dev. 200, 111587. 
  67. Zhang, W., Li, X., Wang, S., Chen, Y., and Liu, H. (2020). Regulation of TFEB activity and its potential as a therapeutic target against kidney diseases. Cell Death Discov. 6, 32. 
  68. Zoncu, R., Bar-Peled, L., Efeyan, A., Wang, S., Sancak, Y., and Sabatini, D.M. (2011). mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase. Science 334, 678-683.  https://doi.org/10.1126/science.1207056