An overview of the role of Wnt signalling pathway in governing transdifferentiation of stem cells towards neuronal lineage
Abstract
Mesenchymal stem cells are found to have the potential to differentiate into many lineages, thus regulating diverse signalling cascades. This unique property of stem cells, called trans differentiation/linear reprogramming, aided in regenerative medicine and tissue repair. The mechanism of such regeneration is still unclear and requires further analysis. Due to the use of external or oncogenic factors, one of the approaches for mending cardiac, renal, and neurological disorders after an injury by induced pluripotent stem cells in the form of reprogramming does not show much benefit in the clinical setting. Consequently, cellular reprogramming may enable the application of clinical research to cell therapy, disease modelling, drug screening, and the fabrication of artificial organs. Studies related to this distinctive phenomenon of stem cells, where the cells could reprogramme themselves into completely different cell lineages, showed a promising future in therapeutic applications. However, unrelenting development in cellular reprogramming has prepared the ways for novel strategies in which signalling pathway manipulation may decide cellular destiny. This cellular reprogramming has got bright prospects in the field of regenerative medicine. Therefore, understanding the relationship between stochasticity and defining cell fate can help decipher molecular regulatory mechanisms of cellular reprogramming.
References
Ahmed, E., Sansac, C., Assou, S., Gras, D., Petit, A., Vachier, I., Chanez, P., De Vos, J., & Bourdin, A. (2018). Lung development, regeneration and plasticity: From disease physiopathology to drug design using induced pluripotent stem cells. Pharmacology & Therapeutics, 183, 58–77. https://doi.org/10.1016/j.pharmthera.2017.10.002
Alvarez-Medina, R., Le Dreau, G., Ros, M., & Martí, E. (2009). Hedgehog activation is required upstream of Wnt signalling to control neural progenitor proliferation. Development (Cambridge, England), 136(19), 3301–3309. https://doi.org/10.1242/dev.041772
Anastas, J. N., & Moon, R. T. (2013). WNT signalling pathways as therapeutic targets in cancer. Nature reviews. Cancer, 13(1), 11–26. https://doi.org/10.1038/nrc3419
Armstrong, R. J., & Svendsen, C. N. (2000). Neural stem cells: from cell biology to cell replacement. Cell Transplantation, 9(2), 139–152. https://doi.org/10.1177/096368970000900202
Atlasi, Y., Noori, R., Gaspar, C., Franken, P., Sacchetti, A., Rafati, H., Mahmoudi, T., Decraene, C., Calin, G. A., Merrill, B. J., & Fodde, R. (2013). Wnt signaling regulates the lineage differentiation potential of mouse embryonic stem cells through Tcf3 down-regulation. PLoS genetics, 9(5), e1003424. https://doi.org/10.1371/journal.pgen.1003424
Banerjee, A., Jothimani, G., Prasad, S. V., Marotta, F., & Pathak, S. (2019). Targeting Wnt Signaling through Small molecules in Governing Stem Cell Fate and Diseases. Endocrine, metabolic & Immune Disorders Drug Targets, 19(3), 233–246. https://doi.org/10.2174/1871530319666190118103907
Barker, N. (2008). The canonical Wnt/beta-catenin signalling pathway. Methods in molecular biology (Clifton, N.J.), 468, 5–15. https://doi.org/10.1007/978-1-59745-249-6_1
Becker, J., & Wilting, J. (2018). WNT signaling, the development of the sympathoadrenal-paraganglionic system and neuroblastoma. Cellular and Molecular Life Sciences : CMLS, 75(6), 1057–1070. https://doi.org/10.1007/s00018-017-2685-8
Bielefeld, P., Schouten, M., Lucassen, P. J., & Fitzsimons, C. P. (2017). Transcription factor oscillations in neural stem cells: Implications for accurate control of gene expression. Neurogenesis (Austin, Tex.), 4(1), e1262934. https://doi.org/10.1080/23262133.2016.1262934
Biswas, S., Chung, S. H., Jiang, P., Dehghan, S., & Deng, W. (2019). Development of glial restricted human neural stem cells for oligodendrocyte differentiation in vitro and in vivo. Scientific Reports, 9(1), 9013. https://doi.org/10.1038/s41598-019-45247-3
Bizen, N., Inoue, T., Shimizu, T., Tabu, K., Kagawa, T., & Taga, T. (2014). A growth-promoting signaling component cyclin D1 in neural stem cells has antiastrogliogenic function to execute self-renewal. Stem cells (Dayton, Ohio), 32(6), 1602–1615.
Black, I. B., & Woodbury, D. (2001). Adult rat and human bone marrow stromal stem cells differentiate into neurons. Blood cells, Molecules & Diseases, 27(3), 632–636. https://doi.org/10.1006/bcmd.2001.0423
Bond, A. M., Bhalala, O. G., & Kessler, J. A. (2012). The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Developmental Neurobiology, 72(7), 1068–1084. https://doi.org/10.1002/dneu.22022
Boulland, J. L., Mastrangelopoulou, M., Boquest, A. C., Jakobsen, R., Noer, A., Glover, J. C., & Collas, P. (2013). Epigenetic regulation of nestin expression during neurogenic differentiation of adipose tissue stem cells. Stem cells and Development, 22(7), 1042–1052. https://doi.org/10.1089/scd.2012.0560
Bowman, A. N., van Amerongen, R., Palmer, T. D., & Nusse, R. (2013). Lineage tracing with Axin2 reveals distinct developmental and adult populations of Wnt/β-catenin-responsive neural stem cells. Proceedings of the National Academy of Sciences of the United States of America, 110(18), 7324–7329. https://doi.org/10.1073/pnas.1305411110
Brederlau, A., Correia, A. S., Anisimov, S. V., Elmi, M., Paul, G., Roybon, L., Morizane, A., Bergquist, F., Riebe, I., Nannmark, U., Carta, M., Hanse, E., Takahashi, J., Sasai, Y., Funa, K., Brundin, P., Eriksson, P. S., & Li, J. Y. (2006). Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem cells (Dayton, Ohio), 24(6), 1433–1440. https://doi.org/10.1634/stemcells.2005-0393
Buchbinder, E. I., & Desai, A. (2016). CTLA-4 and PD-1 Pathways: Similarities, Differences, and Implications of Their Inhibition. American journal of Clinical Oncology, 39(1), 98–106.
https://doi.org/10.1097/COC.0000000000000239
Cable, J., Fuchs, E., Weissman, I., Jasper, H., Glass, D., Rando, T. A., Blau, H., Debnath, S., Oliva, A., Park, S., Passegué, E., Kim, C., & Krasnow, M. A. (2020). Adult stem cells and regenerative medicine-a symposium report. Annals of the New York Academy of Sciences, 1462(1), 27–36. https://doi.org/10.1111/nyas.14243
Cardozo, A. J., Gómez, D. E., & Argibay, P. F. (2012). Neurogenic differentiation of human adipose-derived stem cells: relevance of different signaling molecules, transcription factors, and key marker genes. Gene, 511(2), 427–436. https://doi.org/10.1016/j.gene.2012.09.038
Chen, X., & Li, H. (2022). Neuronal reprogramming in treating spinal cord injury. Neural Regeneration Research, 17(7), 1440–1445. https://doi.org/10.4103/1673-5374.330590
Chiu, A. Y., & Rao, M. S. (2011). Cell-based therapy for neural disorders--anticipating challenges. Neurotherapeutics : The Journal of the American Society for Experimental NeuroTherapeutics, 8(4), 744–752. https://doi.org/10.1007/s13311-011-0066-9
Cho, Y. D., Kim, K. H., Ryoo, H. M., Lee, Y. M., Ku, Y., & Seol, Y. J. (2019). Recent Advances of Useful Cell Sources in the Periodontal Regeneration. Current stem cell research & Therapy, 14(1), 3–8. https://doi.org/10.2174/1574888X13666180816113456
Clevers, H., & Batlle, E. (2006). EphB/EphrinB receptors and Wnt signaling in colorectal cancer. Cancer Research, 66(1), 2–5. https://doi.org/10.1158/0008-5472.CAN-05-3849
Darvishi, M., Tiraihi, T., Mesbah-Namin, S. A., Delshad, A., & Taheri, T. (2017). Motor Neuron Transdifferentiation of Neural Stem Cell from Adipose-Derived Stem Cell Characterized by Differential Gene Expression. Cellular and Molecular Neurobiology, 37(2), 275–289. https://doi.org/10.1007/s10571-016-0368-x
Dezawa, M., Kanno, H., Hoshino, M., Cho, H., Matsumoto, N., Itokazu, Y., Tajima, N., Yamada, H., Sawada, H., Ishikawa, H., Mimura, T., Kitada, M., Suzuki, Y., & Ide, C. (2004). Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. The Journal of Clinical Investigation, 113(12), 1701–1710. https://doi.org/10.1172/JCI20935
Di-Gregorio, A., Sancho, M., Stuckey, D. W., Crompton, L. A., Godwin, J., Mishina, Y., & Rodriguez, T. A. (2007). BMP signalling inhibits premature neural differentiation in the mouse embryo. Development (Cambridge, England), 134(18), 3359–3369. https://doi.org/10.1242/dev.005967
Dorsky, R. I., Moon, R. T., & Raible, D. W. (2000). Environmental signals and cell fate specification in premigratory neural crest. BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology, 22(8), 708–716. https://doi.org/10.1002/1521-1878(200008)22:8<708::AID-BIES4>3.0.CO;2-N
Dravid, G., Ye, Z., Hammond, H., Chen, G., Pyle, A., Donovan, P., Yu, X., & Cheng, L. (2005). Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells (Dayton, Ohio), 23(10), 1489–1501. https://doi.org/10.1634/stemcells.2005-0034
Egawa, N., Suzuki, H., Takahashi, R., Hayakawa, K., Li, W., Lo, E. H., Arai, K., & Inoue, H. (2020). From in vitro to in vivo reprogramming for neural transdifferentiation: An approach for CNS tissue remodeling using stem cell technology. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism, 40(9), 1739–1751. https://doi.org/10.1177/0271678X20910324
Encinas, J. M., & Fitzsimons, C. P. (2017). Gene regulation in adult neural stem cells. Current challenges and possible applications. Advanced Drug Delivery Reviews, 120, 118–132. https://doi.org/10.1016/j.addr.2017.07.016
Etheridge, S. L., Spencer, G. J., Heath, D. J., & Genever, P. G. (2004). Expression profiling and functional analysis of wnt signaling mechanisms in mesenchymal stem cells. Stem Cells (Dayton, Ohio), 22(5), 849–860. https://doi.org/10.1634/stemcells.22-5-849
Fan, J., Wei, Q., Liao, J., Zou, Y., Song, D., Xiong, D., Ma, C., Hu, X., Qu, X., Chen, L., Li, L., Yu, Y., Yu, X., Zhang, Z., Zhao, C., Zeng, Z., Zhang, R., Yan, S., Wu, T., Wu, X., & Tang, H. (2017). Noncanonical Wnt signaling plays an important role in modulating canonical Wnt-regulated stemness, proliferation and terminal differentiation of hepatic progenitors. Oncotarget, 8(16), 27105–27119. https://doi.org/10.18632/oncotarget.15637
Feng, N., Han, Q., Li, J., Wang, S., Li, H., Yao, X., & Zhao, R. C. (2014). Generation of highly purified neural stem cells from human adipose-derived mesenchymal stem cells by Sox1 activation. Stem cells and Development, 23(5), 515–529.
Florian, M. C., Nattamai, K. J., Dörr, K., Marka, G., Uberle, B., Vas, V., Eckl, C., Andrä, I., Schiemann, M., Oostendorp, R. A., Scharffetter-Kochanek, K., Kestler, H. A., Zheng, Y., & Geiger, H. (2013). A canonical to non-canonical Wnt signalling switch in haematopoietic stem-cell ageing. Nature, 503(7476), 392–396. https://doi.org/10.1038/nature12631
Fu, X., Tong, Z., Li, Q., Niu, Q., Zhang, Z., Tong, X., Tong, L., & Zhang, X. (2016). Induction of adipose-derived stem cells into Schwann-like cells and observation of Schwann-like cell proliferation. Molecular Medicine Reports, 14(2), 1187–1193. https://doi.org/10.3892/mmr.2016.5367
Fuchs, E., & Chen, T. (2013). A matter of life and death: self-renewal in stem cells. EMBO Reports, 14(1), 39–48. https://doi.org/10.1038/embor.2012.197
Gentzel, M., Schille, C., Rauschenberger, V., & Schambony, A. (2015). Distinct functionality of dishevelled isoforms on Ca2+/calmodulin-dependent protein kinase 2 (CamKII) in Xenopus gastrulation. Molecular Biology of the Cell, 26(5), 966–977. https://doi.org/10.1091/mbc.E14-06-1089
Giordano, A., Galderisi, U., & Marino, I. R. (2007). From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. Journal of Cellular Physiology, 211(1), 27–35. https://doi.org/10.1002/jcp.20959
Girigoswami, K., Saini, D., & Girigoswami, A. (2021). Extracellular Matrix Remodeling and Development of Cancer. Stem cell Reviews and Reports, 17(3), 739–747. https://doi.org/10.1007/s12015-020-10070-1
Gold, K. S., & Brückner, K. (2014). Drosophila as a model for the two myeloid blood cell systems in vertebrates. Experimental Hematology, 42(8), 717–727. https://doi.org/10.1016/j.exphem.2014.06.002
Gonzalez, D. M., & Medici, D. (2014). Signaling mechanisms of the epithelial-mesenchymal transition. Science Signaling, 7(344), re8. https://doi.org/10.1126/scisignal.2005189
González, F., Boué, S., & Izpisúa Belmonte, J. C. (2011). Methods for making induced pluripotent stem cells: reprogramming à la carte. Nature reviews. Genetics, 12(4), 231–242. https://doi.org/10.1038/nrg2937
González, S., Oh, D., Baclagon, E. R., Zheng, J. J., & Deng, S. X. (2019). Wnt Signaling Is Required for the Maintenance of Human Limbal Stem/Progenitor Cells In Vitro. Investigative Ophthalmology & Visual Science, 60(1), 107–112. https://doi.org/10.1167/iovs.18-25740
Gregorieff, A., Pinto, D., Begthel, H., Destrée, O., Kielman, M., & Clevers, H. (2005). Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology, 129(2), 626–638. https://doi.org/10.1016/j.gastro.2005.06.007
Grijalvo, S., & Díaz, D. D. (2021). Graphene-based hybrid materials as promising scaffolds for peripheral nerve regeneration. Neurochemistry international, 147, 105005. https://doi.org/10.1016/j.neuint.2021.105005
Han, X., Chen, H., Huang, D., Chen, H., Fei, L., Cheng, C., Huang, H., Yuan, G. C., & Guo, G. (2018). Mapping human pluripotent stem cell differentiation pathways using high throughput single-cell RNA-sequencing. Genome Biology, 19(1), 47. https://doi.org/10.1186/s13059-018-1426-0
He, X., Ao, Q., Wei, Y., & Song, J. (2016). Transplantation of miRNA-34a overexpressing adipose-derived stem cell enhances rat nerve regeneration. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society, 24(3), 542–550. https://doi.org/10.1111/wrr.12427
Herman, P. E., Papatheodorou, A., Bryant, S. A., Waterbury, C. K. M., Herdy, J. R., Arcese, A. A., Buxbaum, J. D., Smith, J. J., Morgan, J. R., & Bloom, O. (2018). Highly conserved molecular pathways, including Wnt signaling, promote functional recovery from spinal cord injury in lampreys. Scientific Reports, 8(1), 742. https://doi.org/10.1038/s41598-017-18757-1
Ho, R., Papp, B., Hoffman, J. A., Merrill, B. J., & Plath, K. (2013). Stage-specific regulation of reprogramming to induced pluripotent stem cells by Wnt signaling and T cell factor proteins. Cell Reports, 3(6), 2113–2126. https://doi.org/10.1016/j.celrep.2013.05.015
Hoffmann, A., & Gross, G. (2001). BMP signaling pathways in cartilage and bone formation. Critical reviews in eukaryotic gene expression, 11(1-3), 23–45.
Huang, B., Li, G., & Jiang, X. H. (2015). Fate determination in mesenchymal stem cells: a perspective from histone-modifying enzymes. Stem cell research & therapy, 6(1), 35. https://doi.org/10.1186/s13287-015-0018-0
Huber K. (2006). The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Developmental Biology, 298(2), 335–343. https://doi.org/10.1016/j.ydbio.2006.07.010
Jang, S., Park, J. S., & Jeong, H. S. (2015). Neural Differentiation of Human Adipose Tissue-Derived Stem Cells Involves Activation of the Wnt5a/JNK Signalling. Stem cells International, 2015, 178618. https://doi.org/10.1155/2015/178618
Jothimani, G., Pathak, S., Dutta, S., Duttaroy, A. K., & Banerjee, A. (2022). A Comprehensive Cancer-Associated MicroRNA Expression Profiling and Proteomic Analysis of Human Umbilical Cord Mesenchymal Stem Cell-Derived Exosomes. Tissue engineering and regenerative Medicine, 19(5), 1013–1031. https://doi.org/10.1007/s13770-022-00450-8
Kang S. (2020). Low-density lipoprotein receptor-related protein 6-mediated signaling pathways and associated cardiovascular diseases: diagnostic and therapeutic opportunities. Human Genetics, 139(4), 447–459. https://doi.org/10.1007/s00439-020-02124-8
Katsuda, T., Kosaka, N., Takeshita, F., & Ochiya, T. (2013). The therapeutic potential of mesenchymal stem cell-derived extracellular vesicles. Proteomics, 13(10-11), 1637–1653. https://doi.org/10.1002/pmic.201200373
Kim, J. A., Choi, H. K., Kim, T. M., Leem, S. H., & Oh, I. H. (2015). Regulation of mesenchymal stromal cells through fine tuning of canonical Wnt signaling. Stem cell Research, 14(3), 356–368. https://doi.org/10.1016/j.scr.2015.02.007
Kim, J. B., Zaehres, H., Wu, G., Gentile, L., Ko, K., Sebastiano, V., Araúzo-Bravo, M. J., Ruau, D., Han, D. W., Zenke, M., & Schöler, H. R. (2008). Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature, 454(7204), 646–650. https://doi.org/10.1038/nature07061
Kim, Y., Jeong, J., & Choi, D. (2020). Small-molecule-mediated reprogramming: a silver lining for regenerative medicine. Experimental & Molecular Medicine, 52(2), 213–226. https://doi.org/10.1038/s12276-020-0383-3
Klaus, A., & Birchmeier, W. (2008). Wnt signalling and its impact on development and cancer. Nature reviews. Cancer, 8(5), 387–398. https://doi.org/10.1038/nrc2389
Kléber, M., Lee, H. Y., Wurdak, H., Buchstaller, J., Riccomagno, M. M., Ittner, L. M., Suter, U., Epstein, D. J., & Sommer, L. (2005). Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. The Journal of cell Biology, 169(2), 309–320. https://doi.org/10.1083/jcb.200411095
Knippenberg, M., Helder, M. N., Zandieh Doulabi, B., Wuisman, P. I., & Klein-Nulend, J. (2006). Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochemical and Biophysical Research Communications, 342(3), 902–908. https://doi.org/10.1016/j.bbrc.2006.02.052
Ko, K. H., Holmes, T., Palladinetti, P., Song, E., Nordon, R., O'Brien, T. A., & Dolnikov, A. (2011). GSK-3β inhibition promotes engraftment of ex vivo-expanded hematopoietic stem cells and modulates gene expression. Stem Cells (Dayton, Ohio), 29(1), 108–118. https://doi.org/10.1002/stem.551
Komiya, Y., & Habas, R. (2008). Wnt signal transduction pathways. Organogenesis, 4(2), 68–75. https://doi.org/10.4161/org.4.2.5851
Krabbe, C., Zimmer, J., & Meyer, M. (2005). Neural transdifferentiation of mesenchymal stem cells--a critical review. APMIS : Acta Pathologica, Microbiologica, et Immunologica Scandinavica, 113(11-12), 831–844. https://doi.org/10.1111/j.1600-0463.2005.apm_3061.x
Lai, A. G., & Aboobaker, A. A. (2018). EvoRegen in animals: Time to uncover deep conservation or convergence of adult stem cell evolution and regenerative processes. Developmental Biology, 433(2), 118–131. https://doi.org/10.1016/j.ydbio.2017.10.010
Lento, W., Congdon, K., Voermans, C., Kritzik, M., & Reya, T. (2013). Wnt signaling in normal and malignant hematopoiesis. Cold Spring Harbor Perspectives in Biology, 5(2), a008011. https://doi.org/10.1101/cshperspect.a008011
Lessard, J., Wu, J. I., Ranish, J. A., Wan, M., Winslow, M. M., Staahl, B. T., Wu, H., Aebersold, R., Graef, I. A., & Crabtree, G. R. (2007). An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron, 55(2), 201–215. https://doi.org/10.1016/j.neuron.2007.06.019
Ling, L., Nurcombe, V., & Cool, S. M. (2009). Wnt signaling controls the fate of mesenchymal stem cells. Gene, 433(1-2), 1–7. https://doi.org/10.1016/j.gene.2008.12.008
Liu, J., Sato, C., Cerletti, M., & Wagers, A. (2010). Notch signaling in the regulation of stem cell self-renewal and differentiation. Current topics in Developmental Biology, 92, 367–409. https://doi.org/10.1016/S0070-2153(10)92012-7
Liu, X., Li, F., Stubblefield, E. A., Blanchard, B., Richards, T. L., Larson, G. A., He, Y., Huang, Q., Tan, A. C., Zhang, D., Benke, T. A., Sladek, J. R., Zahniser, N. R., & Li, C. Y. (2012). Direct reprogramming of human fibroblasts into dopaminergic neuron-like cells. Cell Research, 22(2), 321–332. https://doi.org/10.1038/cr.2011.181
López-González, R., & Velasco, I. (2012). Therapeutic potential of motor neurons differentiated from embryonic stem cells and induced pluripotent stem cells. Archives of Medical Research, 43(1), 1–10. https://doi.org/10.1016/j.arcmed.2012.01.007
Luo, L., Hu, D. H., Yin, J. Q., & Xu, R. X. (2018). Molecular Mechanisms of Transdifferentiation of Adipose-Derived Stem Cells into Neural Cells: Current Status and Perspectives. Stem cells International, 2018, 5630802. https://doi.org/10.1155/2018/5630802
Mao, J., Wang, J., Liu, B., Pan, W., Farr, G. H., 3rd, Flynn, C., Yuan, H., Takada, S., Kimelman, D., Li, L., & Wu, D. (2001). Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Molecular Cell, 7(4), 801–809. https://doi.org/10.1016/s1097-2765(01)00224-6
McIntyre, B., Asahara, T., & Alev, C. (2020). Overview of Basic Mechanisms of Notch Signaling in Development and Disease. Advances in Experimental Medicine and Biology, 1227, 9–27. https://doi.org/10.1007/978-3-030-36422-9_2
Memarian, A., Vosough, P., Asgarian-Omran, H., Tabrizi, M., Shabani, M., & Shokri, F. (2012). Differential WNT gene expression in various subtypes of acute lymphoblastic leukemia. Iranian Journal of Immunology : IJI, 9(1), 61–71.
Merrill B. J. (2012). Wnt pathway regulation of embryonic stem cell self-renewal. Cold Spring Harbor Perspectives in Biology, 4(9), a007971. https://doi.org/10.1101/cshperspect.a007971
Miki, T., & Grubbs, B. (2014). Therapeutic potential of placenta-derived stem cells for liver diseases: current status and perspectives. The Journal of Obstetrics and Gynaecology Research, 40(2), 360–368. https://doi.org/10.1111/jog.12213
Noer, A., Sørensen, A. L., Boquest, A. C., & Collas, P. (2006). Stable CpG hypomethylation of adipogenic promoters in freshly isolated, cultured, and differentiated mesenchymal stem cells from adipose tissue. Molecular Biology of the Cell, 17(8), 3543–3556. https://doi.org/10.1091/mbc.e06-04-0322
Nusse R. (2008). Wnt signaling and stem cell control. Cell Research, 18(5), 523–527. https://doi.org/10.1038/cr.2008.47
Oh, S. H., Kim, H. N., Park, H. J., Shin, J. Y., & Lee, P. H. (2015). Mesenchymal Stem Cells Increase Hippocampal Neurogenesis and Neuronal Differentiation by Enhancing the Wnt Signaling Pathway in an Alzheimer's Disease Model. Cell Transplantation, 24(6), 1097–1109. https://doi.org/10.3727/096368914X679237
Ombrato, L., Lluis, F., & Cosma, M. P. (2012). Regulation of self-renewal and reprogramming by TCF factors. Cell cycle (Georgetown, Tex.), 11(1), 39–47. https://doi.org/10.4161/cc.11.1.18759
Pang, Z. P., Yang, N., Vierbuchen, T., Ostermeier, A., Fuentes, D. R., Yang, T. Q., Citri, A., Sebastiano, V., Marro, S., Südhof, T. C., & Wernig, M. (2011). Induction of human neuronal cells by defined transcription factors. Nature, 476(7359), 220–223. https://doi.org/10.1038/nature10202
Parmar, M., Grealish, S., & Henchcliffe, C. (2020). The future of stem cell therapies for Parkinson disease. Nature reviews. Neuroscience, 21(2), 103–115. https://doi.org/10.1038/s41583-019-0257-7
Patel, M., & Yang, S. (2010). Advances in reprogramming somatic cells to induced pluripotent stem cells. Stem cell Reviews and Reports, 6(3), 367–380. https://doi.org/10.1007/s12015-010-9123-8
Petrova, I. M., Malessy, M. J., Verhaagen, J., Fradkin, L. G., & Noordermeer, J. N. (2014). Wnt signaling through the Ror receptor in the nervous system. Molecular Neurobiology, 49(1), 303–315. https://doi.org/10.1007/s12035-013-8520-9
Qin, Y., Zhou, C., Wang, N., Yang, H., & Gao, W. Q. (2015). Conversion of Adipose Tissue-Derived Mesenchymal Stem Cells to Neural Stem Cell-Like Cells by a Single Transcription Factor, Sox2. Cellular Reprogramming, 17(3), 221–226. https://doi.org/10.1089/cell.2015.0001
Rauch, F., Lauzier, D., Croteau, S., Travers, R., Glorieux, F. H., & Hamdy, R. (2000). Temporal and spatial expression of bone morphogenetic protein-2, -4, and -7 during distraction osteogenesis in rabbits. Bone, 27(3), 453–459. https://doi.org/10.1016/s8756-3282(00)00337-9
Richter, J., Traver, D., & Willert, K. (2017). The role of Wnt signaling in hematopoietic stem cell development. Critical reviews in biochemistry and molecular biology, 52(4), 414–424. https://doi.org/10.1080/10409238.2017.1325828
Ringe, J., Kaps, C., Burmester, G. R., & Sittinger, M. (2002). Stem cells for regenerative medicine: advances in the engineering of tissues and organs. Die Naturwissenschaften, 89(8), 338–351. https://doi.org/10.1007/s00114-002-0344-9
Romito, A., & Cobellis, G. (2016). Pluripotent Stem Cells: Current Understanding and Future Directions. Stem cells International, 2016, 9451492. https://doi.org/10.1155/2016/9451492
Roybon, L., Deierborg, T., Brundin, P., & Li, J. Y. (2009). Involvement of Ngn2, Tbr and NeuroD proteins during postnatal olfactory bulb neurogenesis. The European Journal of Neuroscience, 29(2), 232–243. https://doi.org/10.1111/j.1460-9568.2008.06595.x
Sanchez-Ramos, J., Song, S., Cardozo-Pelaez, F., Hazzi, C., Stedeford, T., Willing, A., Freeman, T. B., Saporta, S., Janssen, W., Patel, N., Cooper, D. R., & Sanberg, P. R. (2000). Adult bone marrow stromal cells differentiate into neural cells in vitro. Experimental Neurology, 164(2), 247–256. https://doi.org/10.1006/exnr.2000.7389
Sheikh, A. A., & Groom, J. R. (2021). Transcription tipping points for T follicular helper cell and T-helper 1 cell fate commitment. Cellular & Molecular Immunology, 18(3), 528–538. https://doi.org/10.1038/s41423-020-00554-y
Shenghui, H. E., Nakada, D., & Morrison, S. J. (2009). Mechanisms of stem cell self-renewal. Annual Review of Cell and Developmental, 25, 377-406.
Siebel, C., & Lendahl, U. (2017). Notch Signaling in Development, Tissue Homeostasis, and Disease. Physiological Reviews, 97(4), 1235–1294. https://doi.org/10.1152/physrev.00005.2017
Sineva, G. S., & Pospelov, V. A. (2014). β-Catenin in pluripotency: adhering to self-renewal or Wnting to differentiate?. International Review of cell and Molecular Biology, 312, 53–78. https://doi.org/10.1016/B978-0-12-800178-3.00002-6
Sun, N., Panetta, N. J., Gupta, D. M., Wilson, K. D., Lee, A., Jia, F., Hu, S., Cherry, A. M., Robbins, R. C., Longaker, M. T., & Wu, J. C. (2009). Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells. Proceedings of the National Academy of Sciences of the United States of America, 106(37), 15720–15725. https://doi.org/10.1073/pnas.0908450106
Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126(4), 663–676. https://doi.org/10.1016/j.cell.2006.07.024
Takahashi, K., & Yamanaka, S. (2016). A decade of transcription factor-mediated reprogramming to pluripotency. Nature Reviews. Molecular cell biology, 17(3), 183–193. https://doi.org/10.1038/nrm.2016.8
Tat, P. A., Sumer, H., Jones, K. L., Upton, K., & Verma, P. J. (2010). The efficient generation of induced pluripotent stem (iPS) cells from adult mouse adipose tissue-derived and neural stem cells. Cell Transplantation, 19(5), 525-536. https://doi.org/10.3727/096368910X491374
Taura, D., Noguchi, M., Sone, M., Hosoda, K., Mori, E., Okada, Y., Takahashi, K., Homma, K., Oyamada, N., Inuzuka, M., Sonoyama, T., Ebihara, K., Tamura, N., Itoh, H., Suemori, H., Nakatsuji, N., Okano, H., Yamanaka, S., & Nakao, K. (2009). Adipogenic differentiation of human induced pluripotent stem cells: comparison with that of human embryonic stem cells. FEBS Letters, 583(6), 1029–1033. https://doi.org/10.1016/j.febslet.2009.02.031
Toledo, E. M., Colombres, M., & Inestrosa, N. C. (2008). Wnt signaling in neuroprotection and stem cell differentiation. Progress in Neurobiology, 86(3), 281–296. https://doi.org/10.1016/j.pneurobio.2008.08.001
Tsai, H. L., Deng, W. P., Lai, W. F., Chiu, W. T., Yang, C. B., Tsai, Y. H., Hwang, S. M., & Renshaw, P. F. (2014). Wnts enhance neurotrophin-induced neuronal differentiation in adult bone-marrow-derived mesenchymal stem cells via canonical and noncanonical signaling pathways. PloS One, 9(8), e104937. https://doi.org/10.1371/journal.pone.0104937
Undi, R. B., Gutti, U., Sahu, I., Sarvothaman, S., Pasupuleti, S. R., Kandi, R., & Gutti, R. K. (2016). Wnt Signaling: Role in Regulation of Haematopoiesis. Indian journal of hematology & blood transfusion : an official journal of Indian Society of Hematology and Blood Transfusion, 32(2), 123–134. https://doi.org/10.1007/s12288-015-0585-3
Valkenburg, K. C., Graveel, C. R., Zylstra-Diegel, C. R., Zhong, Z., & Williams, B. O. (2011). Wnt/β-catenin Signaling in Normal and Cancer Stem Cells. Cancers, 3(2), 2050–2079. https://doi.org/10.3390/cancers3022050
Venkatesh, V., Nataraj, R., Thangaraj, G. S., Karthikeyan, M., Gnanasekaran, A., Kaginelli, S. B., Kuppanna, G., Kallappa, C. G., & Basalingappa, K. M. (2018). Targeting Notch signalling pathway of cancer stem cells. Stem cell investigation, 5, 5. https://doi.org/10.21037/sci.2018.02.02
von Rüden, C., Morgenstern, M., Hierholzer, C., Hackl, S., Gradinger, F. L., Woltmann, A., Bühren, V., & Friederichs, J. (2016). The missing effect of human recombinant Bone Morphogenetic Proteins BMP-2 and BMP-7 in surgical treatment of aseptic forearm nonunion. Injury, 47(4), 919–924. https://doi.org/10.1016/j.injury.2015.11.038
Wawersik, S., Evola, C., & Whitman, M. (2005). Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction. Developmental Biology, 277(2), 425–442. https://doi.org/10.1016/j.ydbio.2004.10.002
Wexler, E. M., Paucer, A., Kornblum, H. I., Palmer, T. D., & Geschwind, D. H. (2009). Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells (Dayton, Ohio), 27(5), 1130–1141. https://doi.org/10.1002/stem.36
Wieschaus E. (2016). Positional Information and Cell Fate Determination in the Early Drosophila Embryo. Current topics in developmental biology, 117, 567–579. https://doi.org/10.1016/bs.ctdb.2015.11.020
Wisniewska M. B. (2013). Physiological role of β-catenin/TCF signaling in neurons of the adult brain. Neurochemical Research, 38(6), 1144–1155. https://doi.org/10.1007/s11064-013-0980-9
Wright, K. T., El Masri, W., Osman, A., Chowdhury, J., & Johnson, W. E. (2011). Concise review: Bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem cells (Dayton, Ohio), 29(2), 169–178. https://doi.org/10.1002/stem.570
Xie, M., Tang, S., Li, K., & Ding, S. (2017). Pharmacological Reprogramming of Somatic Cells for Regenerative Medicine. Accounts of Chemical Research, 50(5), 1202–1211. https://doi.org/10.1021/acs.accounts.7b00020
Xie, X., Fu, Y., & Liu, J. (2017). Chemical reprogramming and transdifferentiation. Current opinion in genetics & development, 46, 104–113. https://doi.org/10.1016/j.gde.2017.07.003
Xu, J., Du, Y., & Deng, H. (2015). Direct lineage reprogramming: strategies, mechanisms, and applications. Cell Stem Cell, 16(2), 119–134. https://doi.org/10.1016/j.stem.2015.01.013
Yang, K., Wang, X., Zhang, H., Wang, Z., Nan, G., Li, Y., Zhang, F., Mohammed, M. K., Haydon, R. C., Luu, H. H., Bi, Y., & He, T. C. (2016). The evolving roles of canonical WNT signaling in stem cells and tumorigenesis: implications in targeted cancer therapies. Laboratory Investigation: a Journal of Technical Methods and Pathology, 96(2), 116–136. https://doi.org/10.1038/labinvest.2015.144
Yang, L., Wang, Z. F., Wu, H., & Wang, W. (2018). miR-142-5p Improves Neural Differentiation and Proliferation of Adipose-Derived Stem Cells. Cellular Physiology and Biochemistry : International Journal of Experimental cellular Physiology, Biochemistry, and Pharmacology, 50(6), 2097–2107. https://doi.org/10.1159/000495054
Zakrzewski, W., Dobrzyński, M., Szymonowicz, M., & Rybak, Z. (2019). Stem cells: past, present, and future. Stem cell Research & Therapy, 10(1), 68. https://doi.org/10.1186/s13287-019-1165-5
Zentelytė, A., Žukauskaitė, D., Jacerytė, I., Borutinskaitė, V. V., & Navakauskienė, R. (2021). Small Molecule Treatments Improve Differentiation Potential of Human Amniotic Fluid Stem Cells. Frontiers in Bioengineering and Biotechnology, 9, 623886. https://doi.org/10.3389/fbioe.2021.623886
Zhang, B., Yeo, R. W., Tan, K. H., & Lim, S. K. (2016). Focus on Extracellular Vesicles: Therapeutic Potential of Stem Cell-Derived Extracellular Vesicles. International Journal of Molecular Sciences, 17(2), 174.
https://doi.org/10.3390/ijms17020174
Zhang, Y., & Wang, X. (2020). Targeting the Wnt/β-catenin signaling pathway in cancer. Journal of Hematology & Oncology, 13(1), 165. https://doi.org/10.1186/s13045-020-00990-3
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