Methodology of neuronal pluripotent stem cell of in vitro difference process as an alternative therapy of neurodegenerative disease


Mail Wahyuni Wulansari(1*)
Mail Fuad Gandhi Torizal(2)
Mail Annisa Khumaira(3)
Mail Ika Afifah Nugraheni(4)

(1) Universitas 'Asiyiyah Yogyakarta, Indonesia
(2) Tokyo Medical and Dental University, Japan
(3) Universitas 'Asiyiyah Yogyakarta, Indonesia
(4) Universitas 'Asiyiyah Yogyakarta, Indonesia
(*) Corresponding Author
10.31101/jhes.1730| Abstract views : 452 | PDF views : 208


Neurodegenerative is diseases which occur with age but no therapeutic approach is efficient enough to inhibit neurodegenerative progression which results from aging of the cells themselves. PSC is a stem cell which has the potential to differentiate into various types of cells in the body. In the expansion process, PSC encountered problems, one of the common obstacles. This research was conducted using a literature study method that aims to obtain information about the appropriate differentiation method so that it can be used as an alternative treatment for neurodegenerative disease in the future. The result showed that 3D technique is neuronal differentiation technique that has a good output and can resemble the conditions of its development in vivo. The use of growth factors such as FGF2, PDGF, IGF1, T3, FGF, EGF, and CNTF can also overcome the problem of differentiation of several target cells in neurodegenerative therapy such as neurons, astrocytes, and oligodendrocytes. 


Neuronal stem cell; pluripotent stem cell; differentiation technique

Full Text:



Alghuwainem, A., Alshareeda, A. T., & Alsowayan, B. (2019, Oct 4). Scaffold-Free 3-D Cell Sheet Technique Bridges the Gap between 2-D Cell Culture and Animal Models. Int J Mol Sci, 20(19). https://doi.org/10.3390/ijms20194926

Amira Ragab El Barky, E. A., Tarek M Mohamed. (2017). Stem Cells, Classifications and their Clinical Applications. . Stem cells and development. https://www.researchgate.net/publication/319277041_Stem_Cells_Classifications_and_their_Clinical_Applications

Antoni, D., Burckel, H., Josset, E., & Noel, G. (2015, Mar 11). Three-dimensional cell culture: a breakthrough in vivo. Int J Mol Sci, 16(3), 5517-5527. https://doi.org/10.3390/ijms16035517

Araki, T., Ikegaya, Y., & Koyama, R. (2021, Sep). The effects of microglia- and astrocyte-derived factors on neurogenesis in health and disease. Eur J Neurosci, 54(5), 5880-5901. https://doi.org/10.1111/ejn.14969

Aurélie de Rus Jacquet, H. L. D., Francesca Cicchetti, Melanie Alpaugh. (2021). Current and future applications of induced pluripotent stem cell-based models to study pathological proteins in neurodegenerative disorders. Molecular Psychiatry, 26, pages2685–2706. https://www.nature.com/articles/s41380-020-00999-7

Avila, A., Vidal, P. M., Tielens, S., Morelli, G., Laguesse, S., Harvey, R. J., Rigo, J. M., & Nguyen, L. (2014, Nov). Glycine receptors control the generation of projection neurons in the developing cerebral cortex. Cell Death Differ, 21(11), 1696-1708. https://doi.org/10.1038/cdd.2014.75

Bourgognon, J. M., Spiers, J. G., Scheiblich, H., Antonov, A., Bradley, S. J., Tobin, A. B., & Steinert, J. R. (2018, Aug). Alterations in neuronal metabolism contribute to the pathogenesis of prion disease. Cell Death Differ, 25(8), 1408-1425. https://doi.org/10.1038/s41418-018-0148-x

Cabezas, R., Avila-Rodriguez, M., Vega-Vela, N. E., Echeverria, V., Gonzalez, J., Hidalgo, O. A., Santos, A. B., Aliev, G., & Barreto, G. E. (2016). Growth Factors and Astrocytes Metabolism: Possible Roles for Platelet Derived Growth Factor. Med Chem, 12(3), 204-210. https://doi.org/10.2174/1573406411666151019120444

Carpenter, M. K., Inokuma, M. S., Denham, J., Mujtaba, T., Chiu, C. P., & Rao, M. S. (2001, Dec). Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol, 172(2), 383-397. https://doi.org/10.1006/exnr.2001.7832

Centeno, E. G. Z., Cimarosti, H., & Bithell, A. (2018, May 22). 2D versus 3D human induced pluripotent stem cell-derived cultures for neurodegenerative disease modelling. Mol Neurodegener, 13(1), 27. https://doi.org/10.1186/s13024-018-0258-4

Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M., & Studer, L. (2009, Mar). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol, 27(3), 275-280. https://doi.org/10.1038/nbt.1529

Chandrasekaran, A., Avci, H. X., Leist, M., Kobolak, J., & Dinnyes, A. (2016). Astrocyte Differentiation of Human Pluripotent Stem Cells: New Tools for Neurological Disorder Research. Front Cell Neurosci, 10, 215. https://doi.org/10.3389/fncel.2016.00215

Chang, C. Y., Ting, H. C., Liu, C. A., Su, H. L., Chiou, T. W., Harn, H. J., & Lin, S. Z. (2018, Nov). Induced Pluripotent Stem Cells: A Powerful Neurodegenerative Disease Modeling Tool for Mechanism Study and Drug Discovery. Cell Transplant, 27(11), 1588-1602. https://doi.org/10.1177/0963689718775406

Cunha, C., Panseri, S., & Antonini, S. (2011, Feb). Emerging nanotechnology approaches in tissue engineering for peripheral nerve regeneration. Nanomedicine, 7(1), 50-59. https://doi.org/10.1016/j.nano.2010.07.004

de la Torre-Ubieta, L., & Bonni, A. (2011, Oct 6). Transcriptional regulation of neuronal polarity and morphogenesis in the mammalian brain. Neuron, 72(1), 22-40. https://doi.org/10.1016/j.neuron.2011.09.018

Dhara, S. K., & Stice, S. L. (2008, Oct 15). Neural differentiation of human embryonic stem cells. J Cell Biochem, 105(3), 633-640. https://doi.org/10.1002/jcb.21891

Doss, M. X., & Sachinidis, A. (2019, Apr 30). Current Challenges of iPSC-Based Disease Modeling and Therapeutic Implications. Cells, 8(5). https://doi.org/10.3390/cells8050403

Douvaras, P., Wang, J., Zimmer, M., Hanchuk, S., O'Bara, M. A., Sadiq, S., Sim, F. J., Goldman, J., & Fossati, V. (2014, Aug 12). Efficient generation of myelinating oligodendrocytes from primary progressive multiple sclerosis patients by induced pluripotent stem cells. Stem Cell Reports, 3(2), 250-259. https://doi.org/10.1016/j.stemcr.2014.06.012

Ehrlich, M., Mozafari, S., Glatza, M., Starost, L., Velychko, S., Hallmann, A. L., Cui, Q. L., Schambach, A., Kim, K. P., Bachelin, C., Marteyn, A., Hargus, G., Johnson, R. M., Antel, J., Sterneckert, J., Zaehres, H., Scholer, H. R., Baron-Van Evercooren, A., & Kuhlmann, T. (2017, Mar 14). Rapid and efficient generation of oligodendrocytes from human induced pluripotent stem cells using transcription factors. Proc Natl Acad Sci U S A, 114(11), E2243-E2252. https://doi.org/10.1073/pnas.1614412114

Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., & Sasai, Y. (2008, Nov 6). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell, 3(5), 519-532. https://doi.org/10.1016/j.stem.2008.09.002

Emdad, L., D'Souza, S. L., Kothari, H. P., Qadeer, Z. A., & Germano, I. M. (2012, Feb 10). Efficient differentiation of human embryonic and induced pluripotent stem cells into functional astrocytes. Stem Cells Dev, 21(3), 404-410. https://doi.org/10.1089/scd.2010.0560

Feliciano, D. M., Bordey, A., & Bonfanti, L. (2015, Sep 18). Noncanonical Sites of Adult Neurogenesis in the Mammalian Brain. Cold Spring Harb Perspect Biol, 7(10), a018846. https://doi.org/10.1101/cshperspect.a018846

Gordeeva, O. (2019, Nov 23). TGFbeta Family Signaling Pathways in Pluripotent and Teratocarcinoma Stem Cells' Fate Decisions: Balancing Between Self-Renewal, Differentiation, and Cancer. Cells, 8(12). https://doi.org/10.3390/cells8121500

Gorris, R., Fischer, J., Erwes, K. L., Kesavan, J., Peterson, D. A., Alexander, M., Nothen, M. M., Peitz, M., Quandel, T., Karus, M., & Brustle, O. (2015, Dec). Pluripotent stem cell-derived radial glia-like cells as stable intermediate for efficient generation of human oligodendrocytes. Glia, 63(12), 2152-2167. https://doi.org/10.1002/glia.22882

Gupta, P. K., Das, A. K., Chullikana, A., & Majumdar, A. S. (2012, Jul 9). Mesenchymal stem cells for cartilage repair in osteoarthritis. Stem Cell Res Ther, 3(4), 25. https://doi.org/10.1186/scrt116

Her, G. J., Wu, H. C., Chen, M. H., Chen, M. Y., Chang, S. C., & Wang, T. W. (2013, Feb). Control of three-dimensional substrate stiffness to manipulate mesenchymal stem cell fate toward neuronal or glial lineages. Acta Biomater, 9(2), 5170-5180. https://doi.org/10.1016/j.actbio.2012.10.012

Hopkins, A. M., De Laporte, L., Tortelli, F., Spedden, E., Staii, C., Atherton, T. J., Hubbell, J. A., & Kaplan, D. L. (2013). Silk Hydrogels as Soft Substrates for Neural Tissue Engineering. Advanced Functional Materials, 23(41), 5140-5149. https://doi.org/10.1002/adfm.201300435

Hu, B. Y., Du, Z. W., & Zhang, S. C. (2009). Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc, 4(11), 1614-1622. https://doi.org/10.1038/nprot.2009.186

Hung, C. W., Liou, Y. J., Lu, S. W., Tseng, L. M., Kao, C. L., Chen, S. J., Chiou, S. H., & Chang, C. J. (2010, May 5). Stem cell-based neuroprotective and neurorestorative strategies. Int J Mol Sci, 11(5), 2039-2055. https://doi.org/10.3390/ijms11052039

Izrael, M., Zhang, P., Kaufman, R., Shinder, V., Ella, R., Amit, M., Itskovitz-Eldor, J., Chebath, J., & Revel, M. (2007, Mar). Human oligodendrocytes derived from embryonic stem cells: Effect of noggin on phenotypic differentiation in vitro and on myelination in vivo. Mol Cell Neurosci, 34(3), 310-323. https://doi.org/10.1016/j.mcn.2006.11.008

Jimenez-Moreno, N., Stathakos, P., Caldwell, M. A., & Lane, J. D. (2017, Aug 11). Induced Pluripotent Stem Cell Neuronal Models for the Study of Autophagy Pathways in Human Neurodegenerative Disease. Cells, 6(3). https://doi.org/10.3390/cells6030024

Jinghua Piao, T. M., Gordon Auyeung, Edelweiss Policarpio, Jayanthi Menon, Leif Droms, Philip Gutin, Kunihiro Uryu, Jason Tchieu, Denis Soulet, Viviane Tabar. (2015). Human Embryonic Stem Cell-Derived Oligodendrocyte Progenitors Remyelinate the Brain and Rescue Behavioral Deficits following Radiation. Cell Stem Cell, Pages 198-210. https://www.sciencedirect.com/science/article/pii/S1934590915000053https://www.sciencedirect.com/science/article/pii/S1934590915000053

Keirstead, H. S., Nistor, G., Bernal, G., Totoiu, M., Cloutier, F., Sharp, K., & Steward, O. (2005, May 11). Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci, 25(19), 4694-4705. https://doi.org/10.1523/JNEUROSCI.0311-05.2005

Kempermann, G., Jessberger, S., Steiner, B., & Kronenberg, G. (2004). Milestones of neuronal development in the adult hippocampus. Trends in Neurosciences, 27(8), 447–452. https://doi.org/10.1016/j.tins.2004.05.013

Kim, C., Ho, D. H., Suk, J. E., You, S., Michael, S., Kang, J., Joong Lee, S., Masliah, E., Hwang, D., Lee, H. J., & Lee, S. J. (2013). Neuron-released oligomeric alpha-synuclein is an endogenous agonist of TLR2 for paracrine activation of microglia. Nat Commun, 4, 1562. https://doi.org/10.1038/ncomms2534

Kirkeby, A., Nelander, J., & Parmar, M. (2012). Generating regionalized neuronal cells from pluripotency, a step-by-step protocol. Front Cell Neurosci, 6, 64. https://doi.org/10.3389/fncel.2012.00064

Ko, K. R., & Frampton, J. P. (2016, Jul). Developments in 3D neural cell culture models: the future of neurotherapeutics testing? Expert Rev Neurother, 16(7), 739-741. https://doi.org/10.1586/14737175.2016.1166053

Krencik, R., & Zhang, S. C. (2011, Oct 13). Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat Protoc, 6(11), 1710-1717. https://doi.org/10.1038/nprot.2011.405

Kristiansen, M., & Ham, J. (2014, Jul). Programmed cell death during neuronal development: the sympathetic neuron model. Cell Death Differ, 21(7), 1025-1035. https://doi.org/10.1038/cdd.2014.47

Lafaille, F. G., Pessach, I. M., Zhang, S. Y., Ciancanelli, M. J., Herman, M., Abhyankar, A., Ying, S. W., Keros, S., Goldstein, P. A., Mostoslavsky, G., Ordovas-Montanes, J., Jouanguy, E., Plancoulaine, S., Tu, E., Elkabetz, Y., Al-Muhsen, S., Tardieu, M., Schlaeger, T. M., Daley, G. Q., Abel, L., Casanova, J. L., Studer, L., & Notarangelo, L. D. (2012, Nov 29). Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature, 491(7426), 769-773. https://doi.org/10.1038/nature11583

Lancaster, M. A., & Knoblich, J. A. (2014, Jul 18). Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 345(6194), 1247125. https://doi.org/10.1126/science.1247125

Larijani, B., Esfahani, E. N., Amini, P., Nikbin, B., Alimoghaddam, K., Amiri, S., Malekzadeh, R., Yazdi, N. M., Ghodsi, M., Dowlati, Y., Sahraian, M. A., & Ghavamzadeh, A. (2012). Stem cell therapy in treatment of different diseases. Acta Med Iran, 50(2), 79-96. https://www.ncbi.nlm.nih.gov/pubmed/22359076

Lee, H. K., Velazquez Sanchez, C., Chen, M., Morin, P. J., Wells, J. M., Hanlon, E. B., & Xia, W. (2016). Three Dimensional Human Neuro-Spheroid Model of Alzheimer's Disease Based on Differentiated Induced Pluripotent Stem Cells. PLOS ONE, 11(9), e0163072. https://doi.org/10.1371/journal.pone.0163072

Li, X. J., Du, Z. W., Zarnowska, E. D., Pankratz, M., Hansen, L. O., Pearce, R. A., & Zhang, S. C. (2005, Feb). Specification of motoneurons from human embryonic stem cells. Nat Biotechnol, 23(2), 215-221. https://doi.org/10.1038/nbt1063

Li, Y., Liu, M., Yan, Y., & Yang, S. T. (2014, Jan 26). Neural differentiation from pluripotent stem cells: The role of natural and synthetic extracellular matrix. World J Stem Cells, 6(1), 11-23. https://doi.org/10.4252/wjsc.v6.i1.11

Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Munch, A. E., Chung, W. S., Peterson, T. C., Wilton, D. K., Frouin, A., Napier, B. A., Panicker, N., Kumar, M., Buckwalter, M. S., Rowitch, D. H., Dawson, V. L., Dawson, T. M., Stevens, B., & Barres, B. A. (2017, Jan 26). Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 541(7638), 481-487. https://doi.org/10.1038/nature21029

Liu, G., David, B. T., Trawczynski, M., & Fessler, R. G. (2020, Feb). Advances in Pluripotent Stem Cells: History, Mechanisms, Technologies, and Applications. Stem Cell Rev Rep, 16(1), 3-32. https://doi.org/10.1007/s12015-019-09935-x

Livesey, M. R., Magnani, D., Cleary, E. M., Vasistha, N. A., James, O. T., Selvaraj, B. T., Burr, K., Story, D., Shaw, C. E., Kind, P. C., Hardingham, G. E., Wyllie, D. J., & Chandran, S. (2016, Apr). Maturation and electrophysiological properties of human pluripotent stem cell-derived oligodendrocytes. Stem Cells, 34(4), 1040-1053. https://doi.org/10.1002/stem.2273

Lobsiger, C. S., & Cleveland, D. W. (2007, Nov). Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat Neurosci, 10(11), 1355-1360. https://doi.org/10.1038/nn1988

Lou, Y. R., & Leung, A. W. (2018, Jan - Feb). Next generation organoids for biomedical research and applications. Biotechnol Adv, 36(1), 132-149. https://doi.org/10.1016/j.biotechadv.2017.10.005

McComish, S. F., & Caldwell, M. A. (2018, Jul 5). Generation of defined neural populations from pluripotent stem cells. Philos Trans R Soc Lond B Biol Sci, 373(1750). https://doi.org/10.1098/rstb.2017.0214

Mercurio, S., Serra, L., & Nicolis, S. K. (2019, Sep 13). More than just Stem Cells: Functional Roles of the Transcription Factor Sox2 in Differentiated Glia and Neurons. Int J Mol Sci, 20(18). https://doi.org/10.3390/ijms20184540

Ming, G. L., & Song, H. (2011, May 26). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70(4), 687-702. https://doi.org/10.1016/j.neuron.2011.05.001

Mira, H., & Lie, D. C. (2017, Nov 9). Regulation of Adult Neurogenesis 2.0 - Beyond Signaling Pathways and Transcriptional Regulators. Brain Plast, 3(1), 1-3. https://doi.org/10.3233/BPL-179001

Miyazaki, T., Miyauchi, S., Matsuzaka, S., Yamagishi, C., & Kobayashi, K. (2010, May). Formation of proteoglycan and collagen-rich scaffold-free stiff cartilaginous tissue using two-step culture methods with combinations of growth factors. Tissue Eng Part A, 16(5), 1575-1584. https://doi.org/10.1089/ten.TEA.2009.0443

Mormone, E., D'Sousa, S., Alexeeva, V., Bederson, M. M., & Germano, I. M. (2014, Nov 1). "Footprint-free" human induced pluripotent stem cell-derived astrocytes for in vivo cell-based therapy. Stem Cells Dev, 23(21), 2626-2636. https://doi.org/10.1089/scd.2014.0151

Nolbrant, S., Heuer, A., Parmar, M., & Kirkeby, A. (2017, Sep). Generation of high-purity human ventral midbrain dopaminergic progenitors for in vitro maturation and intracerebral transplantation. Nat Protoc, 12(9), 1962-1979. https://doi.org/10.1038/nprot.2017.078

Oh, Y., & Jang, J. (2019, Mar 31). Directed Differentiation of Pluripotent Stem Cells by Transcription Factors. Mol Cells, 42(3), 200-209. https://doi.org/10.14348/molcells.2019.2439

Oliva, J., Florentino, A., Bardag-Gorce, F., & Niihara, Y. (2019, Mar). Engineering, differentiation and harvesting of human adipose-derived stem cell multilayer cell sheets. Regen Med, 14(3), 151-163. https://doi.org/10.2217/rme-2018-0053

Osborn, L. M., Kamphuis, W., Wadman, W. J., & Hol, E. M. (2016, Sep). Astrogliosis: An integral player in the pathogenesis of Alzheimer's disease. Prog Neurobiol, 144, 121-141. https://doi.org/10.1016/j.pneurobio.2016.01.001

Pankratz, M. T., Li, X. J., Lavaute, T. M., Lyons, E. A., Chen, X., & Zhang, S. C. (2007, Jun). Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells, 25(6), 1511-1520. https://doi.org/10.1634/stemcells.2006-0707

Rosenzweig, E. S., Brock, J. H., Lu, P., Kumamaru, H., Salegio, E. A., Kadoya, K., Weber, J. L., Liang, J. J., Moseanko, R., Hawbecker, S., Huie, J. R., Havton, L. A., Nout-Lomas, Y. S., Ferguson, A. R., Beattie, M. S., Bresnahan, J. C., & Tuszynski, M. H. (2018, May). Restorative effects of human neural stem cell grafts on the primate spinal cord. Nat Med, 24(4), 484-490. https://doi.org/10.1038/nm.4502

Sakthiswary, R., & Raymond, A. A. (2012, Aug 15). Stem cell therapy in neurodegenerative diseases: From principles to practice. Neural Regen Res, 7(23), 1822-1831. https://doi.org/10.3969/j.issn.1673-5374.2012.23.009

Secondo, A., Esposito, A., Petrozziello, T., Boscia, F., Molinaro, P., Tedeschi, V., Pannaccione, A., Ciccone, R., Guida, N., Di Renzo, G., & Annunziato, L. (2018, Dec). Na(+)/Ca(2+) exchanger 1 on nuclear envelope controls PTEN/Akt pathway via nucleoplasmic Ca(2+) regulation during neuronal differentiation. Cell Death Discov, 4, 12. https://doi.org/10.1038/s41420-017-0018-1

Serio, A., Bilican, B., Barmada, S. J., Ando, D. M., Zhao, C., Siller, R., Burr, K., Haghi, G., Story, D., Nishimura, A. L., Carrasco, M. A., Phatnani, H. P., Shum, C., Wilmut, I., Maniatis, T., Shaw, C. E., Finkbeiner, S., & Chandran, S. (2013, Mar 19). Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy. Proc Natl Acad Sci U S A, 110(12), 4697-4702. https://doi.org/10.1073/pnas.1300398110

Shi, Y., Kirwan, P., & Livesey, F. J. (2012, Oct). Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc, 7(10), 1836-1846. https://doi.org/10.1038/nprot.2012.116

Shirazi, R., Zarnani, A. H., Soleimani, M., Abdolvahabi, M. A., Nayernia, K., & Ragerdi Kashani, I. (2012). BMP4 can generate primordial germ cells from bone-marrow-derived pluripotent stem cells. Cell Biol Int, 36(12), 1185-1193. https://doi.org/10.1042/CBI20110651

Simunovic, M., & Brivanlou, A. H. (2017, Mar 15). Embryoids, organoids and gastruloids: new approaches to understanding embryogenesis. Development, 144(6), 976-985. https://doi.org/10.1242/dev.143529

Singh, V. K., Kumar, N., Kalsan, M., Saini, A., & Chandra, R. (2015). Mechanism of Induction: Induced Pluripotent Stem Cells (iPSCs). J Stem Cells, 10(1), 43-62. https://www.ncbi.nlm.nih.gov/pubmed/26665937

Slanzi, A., Iannoto, G., Rossi, B., Zenaro, E., & Constantin, G. (2020). In vitro Models of Neurodegenerative Diseases. Front Cell Dev Biol, 8, 328. https://doi.org/10.3389/fcell.2020.00328

Stacpoole, S. R., Spitzer, S., Bilican, B., Compston, A., Karadottir, R., Chandran, S., & Franklin, R. J. (2013). High yields of oligodendrocyte lineage cells from human embryonic stem cells at physiological oxygen tensions for evaluation of translational biology. Stem Cell Reports, 1(5), 437-450. https://doi.org/10.1016/j.stemcr.2013.09.006

Stappert, L., Klaus, F., & Brustle, O. (2018). MicroRNAs Engage in Complex Circuits Regulating Adult Neurogenesis. Front Neurosci, 12, 707. https://doi.org/10.3389/fnins.2018.00707

Stover, A. E., Brick, D. J., Nethercott, H. E., Banuelos, M. G., Sun, L., O'Dowd, D. K., & Schwartz, P. H. (2013, Oct). Process-based expansion and neural differentiation of human pluripotent stem cells for transplantation and disease modeling. J Neurosci Res, 91(10), 1247-1262. https://doi.org/10.1002/jnr.23245

Tao, Y., & Zhang, S. C. (2016, Nov 3). Neural Subtype Specification from Human Pluripotent Stem Cells. Cell Stem Cell, 19(5), 573-586. https://doi.org/10.1016/j.stem.2016.10.015

Ulrich, D., Muralitharan, R., & Gargett, C. E. (2013, Oct). Toward the use of endometrial and menstrual blood mesenchymal stem cells for cell-based therapies. Expert Opin Biol Ther, 13(10), 1387-1400. https://doi.org/10.1517/14712598.2013.826187

Wang, S., Bates, J., Li, X., Schanz, S., Chandler-Militello, D., Levine, C., Maherali, N., Studer, L., Hochedlinger, K., Windrem, M., & Goldman, S. A. (2013, Feb 7). Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell, 12(2), 252-264. https://doi.org/10.1016/j.stem.2012.12.002

Watanabe, K., Kamiya, D., Nishiyama, A., Katayama, T., Nozaki, S., Kawasaki, H., Watanabe, Y., Mizuseki, K., & Sasai, Y. (2005, Mar). Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci, 8(3), 288-296. https://doi.org/10.1038/nn1402

Yap, M. S., Nathan, K. R., Yeo, Y., Lim, L. W., Poh, C. L., Richards, M., Lim, W. L., Othman, I., & Heng, B. C. (2015). Neural Differentiation of Human Pluripotent Stem Cells for Nontherapeutic Applications: Toxicology, Pharmacology, and In Vitro Disease Modeling. Stem Cells Int, 2015, 105172. https://doi.org/10.1155/2015/105172

Yin, X., Mead, B. E., Safaee, H., Langer, R., Karp, J. M., & Levy, O. (2016, Jan 7). Engineering Stem Cell Organoids. Cell Stem Cell, 18(1), 25-38. https://doi.org/10.1016/j.stem.2015.12.005

Zakrzewski, W., Dobrzynski, M., Szymonowicz, M., & Rybak, Z. (2019, Feb 26). Stem cells: past, present, and future. Stem Cell Res Ther, 10(1), 68. https://doi.org/10.1186/s13287-019-1165-5

Zhang, S. C., Wernig, M., Duncan, I. D., Brüstle, O., & Thomson, J. A. (2011). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nature Biotechnology, 19(12), 1129–1133. https://doi.org/10.1038/nbt1201-1129

DOI: https://doi.org/10.31101/jhes.1730

Article Metrics

Abstract view : 452 times
PDF - 208 times

Cited By


  • There are currently no refbacks.

JHes (Journal of Health Studies)
Indexing by :
Universitas 'Aisyiyah (UNISA) Yogyakarta
Kampus Terpadu: Jl. Siliwangi (Ring Road Barat) No. 63, Nogotirto, Gamping, Sleman, Yogyakarta 55292 
Telepon: (0274) 4469199
Fax.: (0274) 4469204
Email: jhes@unisayogya.ac.id

Statistik: View My Stats

Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.