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08.10.2019 | Original Paper

Driving Neurogenesis in Neural Stem Cells with High Sensitivity Optogenetics

verfasst von: Daniel Boon Loong Teh, Ankshita Prasad, Wenxuan Jiang, Nianchen Zhang, Yang Wu, Hyunsoo Yang, Sanyang Han, Zhigao Yi, Yanzhuang Yeo, Toru Ishizuka, Limsoon Wong, Nitish Thakor, Hiromu Yawo, Xiaogang Liu, Angelo All

Erschienen in: NeuroMolecular Medicine | Ausgabe 1/2020

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Abstract

Optogenetic stimulation of neural stem cells (NSCs) enables their activity-dependent photo-modulation. This provides a spatio-temporal tool for studying activity-dependent neurogenesis and for regulating the differentiation of the transplanted NSCs. Currently, this is mainly driven by viral transfection of channelrhodopsin-2 (ChR2) gene, which requires high irradiance and complex in vivo/vitro stimulation systems. Additionally, despite the extensive application of optogenetics in neuroscience, the transcriptome-level changes induced by optogenetic stimulation of NSCs have not been elucidated yet. Here, we made transformed NSCs (SFO-NSCs) stably expressing one of the step-function opsin (SFO)-variants of chimeric channelrhodopsins, ChRFR(C167A), which is more sensitive to blue light than native ChR2, via a non-viral transfection system using piggyBac transposon. We set up a simple low-irradiance optical stimulation (OS)-incubation system that induced c-fos mRNA expression, which is activity-dependent, in differentiating SFO-NSCs. More neuron-like SFO-NCSs, which had more elongated axons, were differentiated with daily OS than control cells without OS. This was accompanied by positive/negative changes in the transcriptome involved in axonal remodeling, synaptic plasticity, and microenvironment modulation with the up-regulation of several genes involved in the Ca²⁺-related functions. Our approach could be applied for stem cell transplantation studies in tissue with two strengths: lower carcinogenicity and less irradiance needed for tissue penetration.

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Abad, M. A., Enguita, M., DeGregorio-Rocasolano, N., Ferrer, I., & Trullas, R. (2006). Neuronal pentraxin 1 contributes to the neuronal damage evoked by amyloid-beta and is overexpressed in dystrophic neurites in Alzheimer’s brain. Journal of Neuroscience,26(49), 12735–12747. https://doi.org/10.1523/jneurosci.0575-06.2006.CrossRefPubMed

Anderson, M. A., Burda, J. E., Ren, Y., Ao, Y., O’Shea, T. M., Kawaguchi, R., et al. (2016). Astrocyte scar formation aids central nervous system axon regeneration. Nature,532(7598), 195–200. https://doi.org/10.1038/nature17623.CrossRefPubMedPubMedCentral

Bacaj, T., Wu, D., Burre, J., Malenka, R. C., Liu, X., & Sudhof, T. C. (2015). Synaptotagmin-1 and -7 are redundantly essential for maintaining the capacity of the readily-releasable pool of synaptic vesicles. PLoS Biology,13(10), e1002267. https://doi.org/10.1371/journal.pbio.1002267.CrossRefPubMedPubMedCentral

Ben-Arie, N., Bellen, H. J., Armstrong, D. L., McCall, A. E., Gordadze, P. R., Guo, Q., et al. (1997). Math1 is essential for genesis of cerebellar granule neurons. Nature,390(6656), 169–172. https://doi.org/10.1038/36579.CrossRefPubMed

Black, M. M., Slaughter, T., Moshiach, S., Obrocka, M., & Fischer, I. (1996). Tau is enriched on dynamic microtubules in the distal region of growing axons. Journal of Neuroscience,16(11), 3601–3619. https://doi.org/10.1523/JNEUROSCI.16-11-03601.CrossRefPubMed

da Huang, W., Sherman, B. T., & Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols,4(1), 44–57. https://doi.org/10.1038/nprot.2008.211.CrossRef

Daadi, M. M., Klausner, J. Q., Bajar, B., Goshen, I., Lee-Messer, C., Lee, S. Y., et al. (2016). Optogenetic stimulation of neural grafts enhances neurotransmission and downregulates the inflammatory response in experimental stroke model. Cell Transplantation,25(7), 1371–1380. https://doi.org/10.3727/096368915x688533.CrossRefPubMed

D’Ascenzo, M., Piacentini, R., Casalbore, P., Budoni, M., Pallini, R., Azzena, G. B., et al. (2006). Role of L-type Ca²⁺ channels in neural stem/progenitor cell differentiation. European Journal of Neuroscience,23, 935–944. https://doi.org/10.1111/j.1460-9568.2006.04628.x.CrossRef

Dean, C., Liu, H., Dunning, F. M., Chang, P. Y., Jackson, M. B., & Chapman, E. R. (2009). Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nature Neuroscience,12(6), 767–776. https://doi.org/10.1038/nn.2315.CrossRefPubMedPubMedCentral

DeGregorio-Rocasolano, N., Gasull, T., & Trullas, R. (2001). Overexpression of neuronal pentraxin 1 is involved in neuronal death evoked by low K⁺ in cerebellar granule cells. Journal of Biological Chemistry,276(1), 796–803. https://doi.org/10.1074/jbc.M007967200.CrossRef

Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., & Malenka, R. C. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron,42(4), 535–552. https://doi.org/10.1016/S0896-6273(04)00266-1.CrossRefPubMed

Dennis, G., Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., et al. (2003). DAVID: Database for annotation, visualization, and integrated discovery. Genome Biology,4(5), P3.CrossRefPubMed

Gage, F. H., & Temple, S. (2013). Neural stem cells: Generating and regenerating the brain. Neuron,80, 588–601. https://doi.org/10.1016/j.neuron.2013.10.037.CrossRefPubMed

Gerits, A., & Vanduffel, W. (2013). Optogenetics in primates: A shining future? Trends in Genetics,29(7), 403–411. https://doi.org/10.1016/j.tig.2013.03.004.CrossRefPubMed

Guzowski, J. F., Setlow, B., Wagner, E. K., & McGaugh, J. L. (2001). Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. Journal of Neuroscience,21(14), 5089–5098. https://doi.org/10.1523/JNEUROSCI.21-14-05089.2001.CrossRefPubMed

Hososhima, S., Sakai, S., Ishizuka, T., & Yawo, H. (2015). Kinetic evaluation of photosensitivity in bi-stable variants of chimeric channelrhodopsins. PLoS ONE,10(3), e0119558. https://doi.org/10.1371/journal.pone.0119558.CrossRefPubMedPubMedCentral

Igarashi, H., Ikeda, K., Onimaru, H., Kaneko, R., Koizumi, K., Beppu, K., et al. (2018). Targeted expression of step-function opsins in transgenic rats for optogenetic studies. Scientific Reports,8(1), 5435. https://doi.org/10.1038/s41598-018-23810-8.CrossRefPubMedPubMedCentral

Kageyama, R., Shimojo, H., & Ohtsuka, T. (2019). Dynamic control of neural stem cells by bHLH factors. Neuroscience Research,138, 12–18. https://doi.org/10.1016/j.neures.2018.09.005.CrossRefPubMed

Karra, D., & Dahm, R. (2010). Transfection techniques for neuronal cells. Journal of Neuroscience,30(18), 6171–6177. https://doi.org/10.1523/JNEUROSCI.0183-10.2010.CrossRefPubMed

Kastanenka, K. V., & Landmesser, L. T. (2010). In vivo activation of channelrhodopsin-2 reveals that normal patterns of spontaneous activity are required for motoneuron guidance and maintenance of guidance molecules. Journal of Neuroscience,30(31), 10575–10585. https://doi.org/10.1523/JNEUROSCI.2773-10.2010.CrossRefPubMed

Kempermann, G. (2015). Activity dependency and aging in the regulation of adult neurogenesis. Cold Spring Harbor Perspectives in Biology,7(11), a018929. https://doi.org/10.1101/cshperspect.a018929.CrossRefPubMedPubMedCentral

Kim, S. H., Park, Y. R., Lee, B., Choi, B., Kim, H., & Kim, C. H. (2017). Reduction of Cav1.3 channels in dorsal hippocampus impairs the development of dentate gyrus newborn neurons and hippocampal-dependent memory tasks. PLoS ONE,12(7), e0181138. https://doi.org/10.1371/journal.pone.0181138.CrossRefPubMedPubMedCentral

Lacoste, A., Berenshteyn, F., & Brivanlou, A. H. (2009). An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell,5(3), 332–342. https://doi.org/10.1016/j.stem.2009.07.011.CrossRefPubMed

Landeira, B. S., Santana, T. T. D. S., Araújo, J. A. M., Tabet, E. I., Tannous, B. A., Schroeder, T., et al. (2018). Activity-independent effects of CREB on neuronal survival and differentiation during mouse cerebral cortex development. Cerebral Cortex,28(2), 538–548. https://doi.org/10.1093/cercor/bhw387.CrossRefPubMed

Lanier, M. H., Kim, T., & Cooper, J. A. (2015). CARMIL2 is a novel molecular connection between vimentin and actin essential for cell migration and invadopodia formation. Molecular Biology of the Cell,26(25), 4577–4588. https://doi.org/10.1091/mbc.E15-08-0552.CrossRefPubMedPubMedCentral

Li, Z., Michael, I. P., Zhou, D., Nagy, A., & Rini, J. M. (2013). Simple piggyBac transposon-based mammalian cell expression system for inducible protein production. Proceedings of the National Academy of Sciences of the United States of America,110(13), 5004–5009. https://doi.org/10.1073/pnas.1218620110.CrossRefPubMedPubMedCentral

Li, G., & Pleasure, S. J. (2010). Ongoing interplay between the neural network and neurogenesis in the adult hippocampus. Current Opinion in Neurobiology,20(1), 126–133. https://doi.org/10.1016/j.conb.2009.12.008.CrossRefPubMedPubMedCentral

Littleton, J. T., Serano, T. L., Rubin, G. M., Ganetzky, B., & Chapman, E. R. (1999). Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature,400(6746), 757–760. https://doi.org/10.1038/23462.CrossRefPubMed

Livak, K. J., & Schmittgen. T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{{ - \Delta \Delta C_{\text{T}} }}\) method. Methods, 25(4), 402–408, https://doi.org/10.1006/meth.2001.1262 CrossRefPubMed

Marschallinger, J., Sah, A., Schmuckermair, C., Unger, M., Rotheneichner, P., Kharitonova, M., et al. (2015). The L-type calcium channel Cav1.3 is required for proper hippocampal neurogenesis and cognitive functions. Cell Calcium,58(6), 606–616. https://doi.org/10.1016/j.ceca.2015.09.007.CrossRefPubMed

Pallotto, M., & Deprez, F. (2014). Regulation of adult neurogenesis by GABAergic transmission: Signaling beyond GABA_A-receptors. Frontiers in Cellular Neuroscience,8, 166. https://doi.org/10.3389/fncel.2014.00166.CrossRefPubMedPubMedCentral

Schaukowitch, K., Reese, A. L., Kim, S. K., Kilaru, G., Joo, J. Y., Kavalali, E. T., et al. (2017). An intrinsic transcriptional program underlying synaptic scaling during activity suppression. Cell Rep,18(6), 1512–1526. https://doi.org/10.1016/j.celrep.2017.01.033.CrossRefPubMedPubMedCentral

Sidor, M. M., Davidson, T. J., Tye, K. M., Warden, M. R., Diesseroth, K., & McClung, C. A. (2015). In vivo optogenetic stimulation of the rodent central nervous system. Journal of Visualized Experiments,95, e51483. https://doi.org/10.3791/51483.CrossRef

Simms, B. A., & Zamponi, G. W. (2014). Neuronal voltage-gated calcium channels: Structure, function, and dysfunction. Neuron,82, 24–45. https://doi.org/10.1016/j.neuron.2014.03.016.CrossRefPubMed

Srivastava, R., Kumar, M., Peineau, S., Csaba, Z., Mani, S., Gressens, P., et al. (2013). Conditional induction of Math1 specifies embryonic stem cells to cerebellar granule neuron lineage and promotes differentiation into mature granule neurons. Stem Cells,31(4), 652–665. https://doi.org/10.1002/stem.1295.CrossRefPubMed

Steinbeck, J. A., Choi, S. J., Mrejeru, A., Ganat, Y., Deisseroth, K., Sulzer, D., et al. (2015). Optogenetics enables functional analysis of human embryonic stem cell-derived grafts in a Parkinson’s disease model. Nature Biotechnology,33(2), 204–209. https://doi.org/10.1038/nbt.3124.CrossRefPubMedPubMedCentral

Stroh, A., Tsai, H. C., Wang, L. P., Zhang, F., Kressel, J., Aravanis, A., et al. (2011). Tracking stem cell differentiation in the setting of automated optogenetic stimulation. Stem Cells,29(1), 78–88. https://doi.org/10.1002/stem.558.CrossRefPubMedPubMedCentral

Sugiyama, Y., Wang, H., Hikima, T., Sato, M., Kuroda, J., Takahashi, T., et al. (2009). Photocurrent attenuation by a single polar-to-nonpolar point mutation of channelrhodopsin-2. Photochemical & Photobiological Sciences,8(3), 328–336. https://doi.org/10.1039/b815762f.CrossRef

Takahashi, J. (2018). Stem cells and regenerative medicine for neural repair. Current Opinion in Biotechnology,52, 102–108. https://doi.org/10.1016/j.copbio.2018.03.006.CrossRefPubMed

Teh, D. B., Ishizuka, T., & Yawo, H. (2014). Regulation of later neurogenic stages of adult-derived neural stem/progenitor cells by L-type Ca²⁺ channels. Development, Growth & Differentiation,56(8), 583–594. https://doi.org/10.1111/dgd.12158.CrossRef

Tscherter, A., Heidemann, M., Kleinlogel, S., & Streit, J. (2016). Embryonic cell grafts in a culture model of spinal cord lesion: Neuronal relay formation is essential for functional regeneration. Frontiers in Cellular Neuroscience,10, 220. https://doi.org/10.3389/fncel.2016.00220.CrossRefPubMedPubMedCentral

Uchida, H., Morita, T., Niizuma, K., Kushida, Y., Kuroda, Y., Wakao, S., et al. (2016). Transplantation of unique subpopulation of fibroblasts, Muse cells, ameliorates experimental stroke possibly via robust neuronal differentiation. Stem Cells,34(1), 160–173. https://doi.org/10.1002/stem.2206.CrossRefPubMed

Walker, T. L., White, A., Black, D. M., Wallace, R. H., Sah, P., & Bartlett, P. F. (2008). Latent stem and progenitor cells in the hippocampus are activated by neural excitation. Journal of Neuroscience,28(20), 5240–5247. https://doi.org/10.1523/JNEUROSCI.0344-08.2008.CrossRefPubMed

Wang, S. J., Weng, C. H., Xu, H. W., Zhao, C. J., & Yin, Z. Q. (2014). Effect of optogenetic stimulus on the proliferation and cell cycle progression of neural stem cells. Journal of Membrane Biology,247(6), 493–500. https://doi.org/10.1007/s00232-014-9659-7.CrossRefPubMed

West, A. E., Chen, W. G., Dalva, M. B., Dolmetsch, R. E., Kornhauser, J. M., Shaywitz, A. J., et al. (2001). Calcium regulation of neuronal gene expression. Proceedings of the National academy of Sciences of the United States of America,98, 11024–11031. https://doi.org/10.1073/pnas.191352298.CrossRefPubMedPubMedCentral

Wyatt, B. M., Tring, E., & Trachtenberg, J. T. (2012). Pattern and not magnitude of neural activity determines dendritic spine stability in awake mice. Nature Neuroscience,15(7), 949–951. https://doi.org/10.1038/nn.3134.CrossRefPubMedPubMedCentral

Xu, J., Mashimo, T., & Südhof, T. C. (2007). Synaptotagmin-1, -2, and -9: Ca²⁺ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron,54(4), 567–581. https://doi.org/10.1016/j.neuron.2007.05.004.CrossRefPubMed

Yabe, J. T., Wang, F. S., Chylinski, T., Katchmar, T., & Shea, T. B. (2001). Selective accumulation of the high molecular weight neurofilament subunit within the distal region of growing axonal neurites. Cell Motil Cytoskeleton,50(1), 1–12. https://doi.org/10.1002/cm.1037.CrossRefPubMed

Yawo, H., Asano, T., Sakai, S., & Ishizuka, T. (2013). Optogenetic manipulation of neural and non-neural functions. Development, Growth & Differentiation,55(4), 474–490. https://doi.org/10.1111/dgd.12053.CrossRef

Yokose, J., Ishizuka, T., Yoshida, T., Aoki, J., Koyanagi, Y., & Yawo, H. (2011). Lineage analysis of newly generated neurons in organotypic culture of rat hippocampus. Neuroscience Research,69(3), 223–233. https://doi.org/10.1016/j.neures.2010.11.010.CrossRefPubMed

Zamanian, J. L., Xu, L., Foo, L. C., Nouri, N., Zhou, L., Giffard, R. G., et al. (2012). Genomic analysis of reactive astrogliosis. Journal of Neuroscience,32(18), 6391–6410. https://doi.org/10.1523/jneurosci.6221-11.2012.CrossRefPubMed

Titel: Driving Neurogenesis in Neural Stem Cells with High Sensitivity Optogenetics
verfasst von: Daniel Boon Loong Teh
Ankshita Prasad
Wenxuan Jiang
Nianchen Zhang
Yang Wu
Hyunsoo Yang
Sanyang Han
Zhigao Yi
Yanzhuang Yeo
Toru Ishizuka
Limsoon Wong
Nitish Thakor
Hiromu Yawo
Xiaogang Liu
Angelo All
Publikationsdatum: 08.10.2019
Verlag: Springer US
Erschienen in: NeuroMolecular Medicine / Ausgabe 1/2020
Print ISSN: 1535-1084
Elektronische ISSN: 1559-1174
DOI: https://doi.org/10.1007/s12017-019-08573-3

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Driving Neurogenesis in Neural Stem Cells with High Sensitivity Optogenetics

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