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Zinc Maintains Embryonic Stem Cell Pluripotency and Multilineage Differentiation Potential via AKT Activation

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Zinc Maintains Embryonic Stem Cell Pluripotency and Multilineage Differentiation Potential via AKT Activation

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Mnatsakanyan, H.; Sabater I Serra, R.; Salmerón Sánchez, M.; Rico Tortosa, PM. (2019). Zinc Maintains Embryonic Stem Cell Pluripotency and Multilineage Differentiation Potential via AKT Activation. Frontiers in Cell and Developmental Biology. 7:1-17. https://doi.org/10.3389/fcell.2019.00180

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Title: Zinc Maintains Embryonic Stem Cell Pluripotency and Multilineage Differentiation Potential via AKT Activation
Author: Mnatsakanyan, Hayk Sabater i Serra, Roser Salmerón Sánchez, Manuel Rico Tortosa, Patricia María
UPV Unit: Universitat Politècnica de València. Departamento de Física Aplicada - Departament de Física Aplicada
Universitat Politècnica de València. Departamento de Termodinámica Aplicada - Departament de Termodinàmica Aplicada
Universitat Politècnica de València. Departamento de Ingeniería Eléctrica - Departament d'Enginyeria Elèctrica
Universitat Politècnica de València. Centro de Biomateriales e Ingeniería Tisular - Centre de Biomaterials i Enginyeria Tissular
Issued date:
Abstract:
[EN] Embryonic stem cells (ESCs) possess remarkable abilities, as they can differentiate into all cell types (pluripotency) and be self-renewing, giving rise to two identical cells. These characteristics make ESCs a powerful ...[+]
Subjects: Zinc , ZIP7 , Stemness maintenance , Embryonic stem cells (ESC) , AKT
Copyrigths: Reconocimiento (by)
Source:
Frontiers in Cell and Developmental Biology. (eissn: 2296-634X )
DOI: 10.3389/fcell.2019.00180
Publisher:
Frontiers Media SA
Publisher version: https://doi.org/10.3389/fcell.2019.00180
Project ID:
Ministerio de Ciencia, Innovación y Universidades/RTI2018-096794-B-100
EPSRC/EPSRC-EP/P001114/1
Thanks:
PR acknowledges support from the Spanish Ministry of Science, Innovation and Universities (RTI2018-096794), and Fondo Europeo de Desarrollo Regional (FEDER). CIBER-BBN was an initiative funded by the VI National R&D&I Plan ...[+]
Type: Artículo

References

Anzellotti, A. I., & Farrell, N. P. (2008). Zinc metalloproteins as medicinal targets. Chemical Society Reviews, 37(8), 1629. doi:10.1039/b617121b

Armstrong, L., Hughes, O., Yung, S., Hyslop, L., Stewart, R., Wappler, I., … Lako, M. (2006). The role of PI3K/AKT, MAPK/ERK and NFκβ signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Human Molecular Genetics, 15(11), 1894-1913. doi:10.1093/hmg/ddl112

Bechard, M., & Dalton, S. (2009). Subcellular Localization of Glycogen Synthase Kinase 3β Controls Embryonic Stem Cell Self-Renewal. Molecular and Cellular Biology, 29(8), 2092-2104. doi:10.1128/mcb.01405-08 [+]
Anzellotti, A. I., & Farrell, N. P. (2008). Zinc metalloproteins as medicinal targets. Chemical Society Reviews, 37(8), 1629. doi:10.1039/b617121b

Armstrong, L., Hughes, O., Yung, S., Hyslop, L., Stewart, R., Wappler, I., … Lako, M. (2006). The role of PI3K/AKT, MAPK/ERK and NFκβ signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Human Molecular Genetics, 15(11), 1894-1913. doi:10.1093/hmg/ddl112

Bechard, M., & Dalton, S. (2009). Subcellular Localization of Glycogen Synthase Kinase 3β Controls Embryonic Stem Cell Self-Renewal. Molecular and Cellular Biology, 29(8), 2092-2104. doi:10.1128/mcb.01405-08

Ten Berge, D., Kurek, D., Blauwkamp, T., Koole, W., Maas, A., Eroglu, E., … Nusse, R. (2011). Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nature Cell Biology, 13(9), 1070-1075. doi:10.1038/ncb2314

Cardone, M. H. (1998). Regulation of Cell Death Protease Caspase-9 by Phosphorylation. Science, 282(5392), 1318-1321. doi:10.1126/science.282.5392.1318

Chen, S., Do, J. T., Zhang, Q., Yao, S., Yan, F., Peters, E. C., … Ding, S. (2006). Self-renewal of embryonic stem cells by a small molecule. Proceedings of the National Academy of Sciences, 103(46), 17266-17271. doi:10.1073/pnas.0608156103

Clevers, H. (2016). Modeling Development and Disease with Organoids. Cell, 165(7), 1586-1597. doi:10.1016/j.cell.2016.05.082

Cohen, L., Sekler, I., & Hershfinkel, M. (2014). The zinc sensing receptor, ZnR/GPR39, controls proliferation and differentiation of colonocytes and thereby tight junction formation in the colon. Cell Death & Disease, 5(6), e1307-e1307. doi:10.1038/cddis.2014.262

Czechanski, A., Byers, C., Greenstein, I., Schrode, N., Donahue, L. R., Hadjantonakis, A.-K., & Reinholdt, L. G. (2014). Derivation and characterization of mouse embryonic stem cells from permissive and nonpermissive strains. Nature Protocols, 9(3), 559-574. doi:10.1038/nprot.2014.030

Doble, B. W. (2003). GSK-3: tricks of the trade for a multi-tasking kinase. Journal of Cell Science, 116(7), 1175-1186. doi:10.1242/jcs.00384

Eiselleova, L., Matulka, K., Kriz, V., Kunova, M., Schmidtova, Z., Neradil, J., … Dvorak, P. (2009). A Complex Role for FGF-2 in Self-Renewal, Survival, and Adhesion of Human Embryonic Stem Cells. Stem Cells, 27(8), 1847-1857. doi:10.1002/stem.128

Evans, M. (2011). Discovering pluripotency: 30 years of mouse embryonic stem cells. Nature Reviews Molecular Cell Biology, 12(10), 680-686. doi:10.1038/nrm3190

Evseenko, D., Zhu, Y., Schenke-Layland, K., Kuo, J., Latour, B., Ge, S., … Crooks, G. M. (2010). Mapping the first stages of mesoderm commitment during differentiation of human embryonic stem cells. Proceedings of the National Academy of Sciences, 107(31), 13742-13747. doi:10.1073/pnas.1002077107

Fang, X., Yu, S. X., Lu, Y., Bast, R. C., Woodgett, J. R., & Mills, G. B. (2000). Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proceedings of the National Academy of Sciences, 97(22), 11960-11965. doi:10.1073/pnas.220413597

Fischer, A. H., Jacobson, K. A., Rose, J., & Zeller, R. (2008). Hematoxylin and Eosin Staining of Tissue and Cell Sections. Cold Spring Harbor Protocols, 2008(6), pdb.prot4986-pdb.prot4986. doi:10.1101/pdb.prot4986

Franke, T. F. (2008). PI3K/Akt: getting it right matters. Oncogene, 27(50), 6473-6488. doi:10.1038/onc.2008.313

Hamatake, M., Iguchi, K., Hirano, K., & Ishida, R. (2000). Zinc Induces Mixed Types of Cell Death, Necrosis, and Apoptosis, in Molt-4 Cells. Journal of Biochemistry, 128(6), 933-939. doi:10.1093/oxfordjournals.jbchem.a022844

Hamilton, W. B., & Brickman, J. M. (2014). Erk Signaling Suppresses Embryonic Stem Cell Self-Renewal to Specify Endoderm. Cell Reports, 9(6), 2056-2070. doi:10.1016/j.celrep.2014.11.032

Heo, J., Lee, J.-S., Chu, I.-S., Takahama, Y., & Thorgeirsson, S. S. (2005). Spontaneous differentiation of mouse embryonic stem cells in vitro: Characterization by global gene expression profiles. Biochemical and Biophysical Research Communications, 332(4), 1061-1069. doi:10.1016/j.bbrc.2005.04.173

Hogstrand, C., Kille, P., Nicholson, R. I., & Taylor, K. M. (2009). Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends in Molecular Medicine, 15(3), 101-111. doi:10.1016/j.molmed.2009.01.004

Hu, J., Yang, Z., Wang, J., Yu, J., Guo, J., Liu, S., … Cheng, J. (2016). Zinc Chloride Transiently Maintains Mouse Embryonic Stem Cell Pluripotency by Activating Stat3 Signaling. PLOS ONE, 11(2), e0148994. doi:10.1371/journal.pone.0148994

Huang, L., Kirschke, C. P., Zhang, Y., & Yu, Y. Y. (2005). The ZIP7 Gene (Slc39a7) Encodes a Zinc Transporter Involved in Zinc Homeostasis of the Golgi Apparatus. Journal of Biological Chemistry, 280(15), 15456-15463. doi:10.1074/jbc.m412188200

Jaenisch, R., & Young, R. (2008). Stem Cells, the Molecular Circuitry of Pluripotency and Nuclear Reprogramming. Cell, 132(4), 567-582. doi:10.1016/j.cell.2008.01.015

Jeong, C.-H., Cho, Y.-Y., Kim, M.-O., Kim, S.-H., Cho, E.-J., Lee, S.-Y., … Dong, Z. (2010). Phosphorylation of Sox2 Cooperates in Reprogramming to Pluripotent Stem Cells. STEM CELLS, 28(12), 2141-2150. doi:10.1002/stem.540

Jo, H., Mondal, S., Tan, D., Nagata, E., Takizawa, S., Sharma, A. K., … Luo, H. R. (2012). Small molecule-induced cytosolic activation of protein kinase Akt rescues ischemia-elicited neuronal death. Proceedings of the National Academy of Sciences, 109(26), 10581-10586. doi:10.1073/pnas.1202810109

Johnson-Farley, N. N., Patel, K., Kim, D., & Cowen, D. S. (2007). Interaction of FGF-2 with IGF-1 and BDNF in stimulating Akt, ERK, and neuronal survival in hippocampal cultures. Brain Research, 1154, 40-49. doi:10.1016/j.brainres.2007.04.026

Kattman, S. J., Witty, A. D., Gagliardi, M., Dubois, N. C., Niapour, M., Hotta, A., … Keller, G. (2011). Stage-Specific Optimization of Activin/Nodal and BMP Signaling Promotes Cardiac Differentiation of Mouse and Human Pluripotent Stem Cell Lines. Cell Stem Cell, 8(2), 228-240. doi:10.1016/j.stem.2010.12.008

Kennedy, S. G., Wagner, A. J., Conzen, S. D., Jordan, J., Bellacosa, A., Tsichlis, P. N., & Hay, N. (1997). The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes & Development, 11(6), 701-713. doi:10.1101/gad.11.6.701

Kim, E., Kim, M., Woo, D.-H., Shin, Y., Shin, J., Chang, N., … Lee, J. (2013). Phosphorylation of EZH2 Activates STAT3 Signaling via STAT3 Methylation and Promotes Tumorigenicity of Glioblastoma Stem-like Cells. Cancer Cell, 23(6), 839-852. doi:10.1016/j.ccr.2013.04.008

Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S., & Smith, A. (2007). FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development, 134(16), 2895-2902. doi:10.1242/dev.02880

Lanner, F., & Rossant, J. (2010). The role of FGF/Erk signaling in pluripotent cells. Development, 137(20), 3351-3360. doi:10.1242/dev.050146

Li, W., & Ding, S. (2010). Small molecules that modulate embryonic stem cell fate and somatic cell reprogramming. Trends in Pharmacological Sciences, 31(1), 36-45. doi:10.1016/j.tips.2009.10.002

Lin, Y., Yang, Y., Li, W., Chen, Q., Li, J., Pan, X., … Wang, Y.-J. (2012). Reciprocal Regulation of Akt and Oct4 Promotes the Self-Renewal and Survival of Embryonal Carcinoma Cells. Molecular Cell, 48(4), 627-640. doi:10.1016/j.molcel.2012.08.030

Llames, S., García-Pérez, E., Meana, Á., Larcher, F., & del Río, M. (2015). Feeder Layer Cell Actions and Applications. Tissue Engineering Part B: Reviews, 21(4), 345-353. doi:10.1089/ten.teb.2014.0547

Manning, B. D., & Cantley, L. C. (2007). AKT/PKB Signaling: Navigating Downstream. Cell, 129(7), 1261-1274. doi:10.1016/j.cell.2007.06.009

Morgani, S. M., Canham, M. A., Nichols, J., Sharov, A. A., Migueles, R. P., Ko, M. S. H., & Brickman, J. M. (2013). Totipotent Embryonic Stem Cells Arise in Ground-State Culture Conditions. Cell Reports, 3(6), 1945-1957. doi:10.1016/j.celrep.2013.04.034

Murakami, M., & Hirano, T. (2008). Intracellular zinc homeostasis and zinc signaling. Cancer Science, 99(8), 1515-1522. doi:10.1111/j.1349-7006.2008.00854.x

Murray, P., & Edgar, D. (2001). The regulation of embryonic stem cell differentiation by leukaemia inhibitory factor (LIF). Differentiation, 68(4-5), 227-234. doi:10.1046/j.1432-0436.2001.680410.x

Nair, G., Abranches, E., Guedes, A. M. V., Henrique, D., & Raj, A. (2015). Heterogeneous lineage marker expression in naive embryonic stem cells is mostly due to spontaneous differentiation. Scientific Reports, 5(1). doi:10.1038/srep13339

Niwa, H. (2007). How is pluripotency determined and maintained? Development, 134(4), 635-646. doi:10.1242/dev.02787

Niwa, H., Burdon, T., Chambers, I., & Smith, A. (1998). Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes & Development, 12(13), 2048-2060. doi:10.1101/gad.12.13.2048

Ohtsuka, S., & Dalton, S. (2007). Molecular and biological properties of pluripotent embryonic stem cells. Gene Therapy, 15(2), 74-81. doi:10.1038/sj.gt.3303065

Oshimori, N., & Fuchs, E. (2012). The Harmonies Played by TGF-β in Stem Cell Biology. Cell Stem Cell, 11(6), 751-764. doi:10.1016/j.stem.2012.11.001

Pera, M. F., & Tam, P. P. L. (2010). Extrinsic regulation of pluripotent stem cells. Nature, 465(7299), 713-720. doi:10.1038/nature09228

Rose-John, S. (2002). GP130 stimulation and the maintenance of stem cells. Trends in Biotechnology, 20(10), 417-419. doi:10.1016/s0167-7799(02)02056-5

Saxe, J. P., Tomilin, A., Schöler, H. R., Plath, K., & Huang, J. (2009). Post-Translational Regulation of Oct4 Transcriptional Activity. PLoS ONE, 4(2), e4467. doi:10.1371/journal.pone.0004467

Schugar, R. C., Robbins, P. D., & Deasy, B. M. (2007). Small molecules in stem cell self-renewal and differentiation. Gene Therapy, 15(2), 126-135. doi:10.1038/sj.gt.3303062

Shao, Y., Wolf, P. G., Guo, S., Guo, Y., Gaskins, H. R., & Zhang, B. (2017). Zinc enhances intestinal epithelial barrier function through the PI3K/AKT/mTOR signaling pathway in Caco-2 cells. The Journal of Nutritional Biochemistry, 43, 18-26. doi:10.1016/j.jnutbio.2017.01.013

Singhal, P. K., Sassi, S., Lan, L., Au, P., Halvorsen, S. C., Fukumura, D., … Seed, B. (2015). Mouse embryonic fibroblasts exhibit extensive developmental and phenotypic diversity. Proceedings of the National Academy of Sciences, 113(1), 122-127. doi:10.1073/pnas.1522401112

Stewart, M. H., Bendall, S. C., & Bhatia, M. (2008). Deconstructing human embryonic stem cell cultures: niche regulation of self-renewal and pluripotency. Journal of Molecular Medicine, 86(8), 875-886. doi:10.1007/s00109-008-0356-9

Tamm, C., Pijuan Galitó, S., & Annerén, C. (2013). A Comparative Study of Protocols for Mouse Embryonic Stem Cell Culturing. PLoS ONE, 8(12), e81156. doi:10.1371/journal.pone.0081156

Taylor, K. M., Hiscox, S., Nicholson, R. I., Hogstrand, C., & Kille, P. (2012). Protein Kinase CK2 Triggers Cytosolic Zinc Signaling Pathways by Phosphorylation of Zinc Channel ZIP7. Science Signaling, 5(210), ra11-ra11. doi:10.1126/scisignal.2002585

Taylor, K. M., Vichova, P., Jordan, N., Hiscox, S., Hendley, R., & Nicholson, R. I. (2008). ZIP7-Mediated Intracellular Zinc Transport Contributes to Aberrant Growth Factor Signaling in Antihormone-Resistant Breast Cancer Cells. Endocrinology, 149(10), 4912-4920. doi:10.1210/en.2008-0351

Tremml, G., Singer, M., & Malavarca, R. (2008). Culture of Mouse Embryonic Stem Cells. Current Protocols in Stem Cell Biology, 5(1). doi:10.1002/9780470151808.sc01c04s5

Wang, E. S., Reyes, N. A., Melton, C., Huskey, N. E., Momcilovic, O., Goga, A., … Oakes, S. A. (2015). Fas-Activated Mitochondrial Apoptosis Culls Stalled Embryonic Stem Cells to Promote Differentiation. Current Biology, 25(23), 3110-3118. doi:10.1016/j.cub.2015.10.020

Watanabe, S., Umehara, H., Murayama, K., Okabe, M., Kimura, T., & Nakano, T. (2006). Activation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cells. Oncogene, 25(19), 2697-2707. doi:10.1038/sj.onc.1209307

Weinberger, L., Ayyash, M., Novershtern, N., & Hanna, J. H. (2015). Dynamic stem cell states: naive to primed pluripotency in rodents and humans. doi:10.1101/030676

West, J. A., Park, I.-H., Daley, G. Q., & Geijsen, N. (2006). In vitro generation of germ cells from murine embryonic stem cells. Nature Protocols, 1(4), 2026-2036. doi:10.1038/nprot.2006.303

Wichterle, H., Lieberam, I., Porter, J. A., & Jessell, T. M. (2002). Directed Differentiation of Embryonic Stem Cells into Motor Neurons. Cell, 110(3), 385-397. doi:10.1016/s0092-8674(02)00835-8

Xu, Z., Robitaille, A. M., Berndt, J. D., Davidson, K. C., Fischer, K. A., Mathieu, J., … Moon, R. T. (2016). Wnt/β-catenin signaling promotes self-renewal and inhibits the primed state transition in naïve human embryonic stem cells. Proceedings of the National Academy of Sciences, 113(42), E6382-E6390. doi:10.1073/pnas.1613849113

Yamaguchi, H., & Wang, H.-G. (2001). The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene, 20(53), 7779-7786. doi:10.1038/sj.onc.1204984

Yamasaki, S., Sakata-Sogawa, K., Hasegawa, A., Suzuki, T., Kabu, K., Sato, E., … Hirano, T. (2007). Zinc is a novel intracellular second messenger. Journal of Cell Biology, 177(4), 637-645. doi:10.1083/jcb.200702081

Yiangou, L., Ross, A. D. B., Goh, K. J., & Vallier, L. (2018). Human Pluripotent Stem Cell-Derived Endoderm for Modeling Development and Clinical Applications. Cell Stem Cell, 22(4), 485-499. doi:10.1016/j.stem.2018.03.016

Yu, J. S. L., & Cui, W. (2016). Proliferation, survival and metabolism: the role of PI3K/AKT/mTOR signalling in pluripotency and cell fate determination. Development, 143(17), 3050-3060. doi:10.1242/dev.137075

Zhou, J., Wulfkuhle, J., Zhang, H., Gu, P., Yang, Y., Deng, J., … Zhang, Y. (2007). Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proceedings of the National Academy of Sciences, 104(41), 16158-16163. doi:10.1073/pnas.0702596104

Ziomek, C. A., Lepire, M. L., & Torres, I. (1990). A highly fluorescent simultaneous azo dye technique for demonstration of nonspecific alkaline phosphatase activity. Journal of Histochemistry & Cytochemistry, 38(3), 437-442. doi:10.1177/38.3.1689343

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