Browse > Article
http://dx.doi.org/10.5352/JLS.2019.29.12.1329

Effects of Transient Treatment with Rotenone, a Mitochondrial Inhibitor, on Mouse Subventricular Zone Neural Stem Cells  

Park, Ki-Youb (Korea Science Academy of KAIST)
Kim, Man Su (College of Pharmacy, Inje University)
Publication Information
Journal of Life Science / v.29, no.12, 2019 , pp. 1329-1336 More about this Journal
Abstract
Subventricular zone (SVZ) in the brain contains neural stem cells (NSCs) which self-renew and differentiate to neurons and glial cells during postnatal period and throughout adulthood. Since fate decision to either proliferation or differentiation has to respond to intracellular and extracellular conditions, many intrinsic and extrinsic factors are involved. Among them, mitochondria have been reported to participate in fate decision of NSCs. In our previous report, we showed that long-term treatment of a mitochondrial inhibitor rotenone greatly inhibited neurogenesis. In this study, we examined the effects of short-term treatment of rotenone on SVZ NSCs. We found that (1) even one-day treatment of rotenone significantly reduced neurogenesis and earlier time points seemed to be more sensitive to rotenone, (2) a number of Mash1+ transit amplifying cells was decreased by one-day treatment of rotenone, (3) short-term treatment of rotenone eliminated most of the differentiated Tuj1+ neurons and Olig2+ oligodendrocytes, while glial fibrillary acidic protein (GFAP)+ astrocytes were not affected, and (4) sulfiredoxin 1 (Srxn1) gene expression was increased after one-day treatment of rotenone, indicating activation of nuclear factor (erythroid-derived 2)-like 2 (Nrf2) pathway. All these results confirm that functional mitochondria are necessary during differentiation to neurons or oligodendrocytes as well as maintenance of neurons after differentiation. Also, these data suggest that temporary exposure to mitochondrial inhibitor such as rotenone might have long-term effects on neurogenic potential of NSCs.
Keywords
Mitochondria; neural stem cells (NSCs); neuronal differentiation; rotenone; subventricular zone (SVZ);
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Richetin, K., Moulis, M., Millet, A., Arrazola, M. S., Andraini, T., Hua, J., Davezac, N., Roybon, L., Belenguer, P., Miquel, M. C. and Rampon, C. 2017. Amplifying mitochondrial function rescues adult neurogenesis in a mouse model of alzheimer's disease. Neurobiol. Dis. 102, 113-124.   DOI
2 Shaw, P. and Chattopadhyay, A. 2019. Nrf2-ARE signaling in cellular protection: Mechanism of action and the regulatory mechanisms. J. Cell. Physiol. doi:10.1002/jcp.29219.
3 Son, G. and Han, J. 2018. Roles of mitochondria in neuronal development. BMB Rep. 51, 549-556.   DOI
4 von Wrangel, C., Schwabe, K., John, N., Krauss, J. K. and Alam, M. 2015. The rotenone-induced rat model of parkinson's disease: Behavioral and electrophysiological findings. Behav. Brain Res. 279, 52-61.   DOI
5 Walter, J., Bolognin, S., Antony, P. M. A., Nickels, S. L., Poovathingal, S. K., Salamanca, L., Magni, S., Perfeito, R., Hoel, F., Qing, X., Jarazo, J., Arias-Fuenzalida, J., Ignac, T., Monzel, A. S., Gonzalez-Cano, L., Pereira de Almeida, L., Skupin, A., Tronstad, K. J. and Schwamborn, J. C. 2019. Neural stem cells of parkinson's disease patients exhibit aberrant mitochondrial morphology and functionality. Stem Cell Reports 12, 878-889.   DOI
6 Wu, J., Chen, Y., Yu, S., Li, L., Zhao, X., Li, Q., Zhao, J. and Zhao, Y. 2017. Neuroprotective effects of sulfiredoxin-1 during cerebral ischemia/reperfusion oxidative stress injury in rats. Brain Res. Bull. 132, 99-108.   DOI
7 Zhou, Y., Duan, S., Zhou, Y., Yu, S., Wu, J., Wu, X., Zhao, J. and Zhao, Y. 2015. Sulfiredoxin-1 attenuates oxidative stress via nrf2/are pathway and 2-cys prdxs after oxygenglucose deprivation in astrocytes. J. Mol. Neurosci. 55, 941-950.   DOI
8 Corenblum, M. J., Ray, S., Remley, Q. W., Long, M., Harder, B., Zhang, D. D., Barnes, C. A. and Madhavan, L. 2016. Reduced nrf2 expression mediates the decline in neural stem cell function during a critical middle-age period. Aging Cell 15, 725-736.   DOI
9 Cabezas, R., Vega-Vela, N. E., Gonzalez-Sanmiguel, J., Gonzalez, J., Esquinas, P., Echeverria, V. and Barreto, G. E. 2018. Pdgf-bb preserves mitochondrial morphology, attenuates ros production, and upregulates neuroglobin in an astrocytic model under rotenone insult. Mol. Neurobiol. 55, 3085-3095.   DOI
10 Choi, S. Y., Kim, J. Y., Kim, H. W., Cho, B., Cho, H. M., Oppenheim, R. W., Kim, H., Rhyu, I. J. and Sun, W. 2013. Drp1-mediated mitochondrial dynamics and survival of developing chick motoneurons during the period of normal programmed cell death. FASEB J. 27, 51-62.   DOI
11 Hayes, J. D., McMahon, M., Chowdhry, S. and Dinkova-Kostova, A. T. 2010. Cancer chemoprevention mechanisms mediated through the keap1-nrf2 pathway. Antioxid. Redox Signal. 13, 1713-1748.   DOI
12 Park, K. Y. and Kim, M. S. 2018. Inhibition of proliferation and neurogenesis of mouse subventricular zone neural stem cells by a mitochondrial inhibitor rotenone. J. Life Sci. 28, 1397-1405.   DOI
13 Lu, J., Li, Y., Mollinari, C., Garaci, E., Merlo, D. and Pei, G. 2019. Amyloid-beta oligomers-induced mitochondrial DNA repair impairment contributes to altered human neural stem cell differentiation. Curr. Alzheimer Res. 16, 934-949.   DOI
14 Kim, E. J., Ables, J. L., Dickel, L. K., Eisch, A. J. and Johnson, J. E. 2011. Ascl1 (mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS One 6, e18472.   DOI
15 Kim, H. J., Shaker, M. R., Cho, B., Cho, H. M., Kim, H., Kim, J. Y. and Sun, W. 2015. Dynamin-related protein 1 controls the migration and neuronal differentiation of subventricular zone-derived neural progenitor cells. Sci. Rep. 5, 15962.   DOI
16 Krug, A. K., Balmer, N. V., Matt, F., Schonenberger, F., Merhof, D. and Leist, M. 2013. Evaluation of a human neurite growth assay as specific screen for developmental neurotoxicants. Arch. Toxicol. 87, 2215-2231.   DOI
17 L'Episcopo, F., Tirolo, C., Testa, N., Caniglia, S., Morale, M. C., Impagnatiello, F., Pluchino, S. and Marchetti, B. 2013. Aging-induced nrf2-are pathway disruption in the subventricular zone drives neurogenic impairment in parkinsonian mice via pi3k-wnt/beta-catenin dysregulation. J. Neurosci. 33, 1462-1485.   DOI
18 Lim, D. A. and Alvarez-Buylla, A. 2016. The adult ventricular-subventricular zone (v-svz) and olfactory bulb (ob) neurogenesis. Cold Spring Harb. Perspect. Biol. 8, a018820.   DOI
19 Ma, Q. 2013. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53, 401-426.   DOI
20 Nakatani, H., Martin, E., Hassani, H., Clavairoly, A., Maire, C. L., Viadieu, A., Kerninon, C., Delmasure, A., Frah, M., Weber, M., Nakafuku, M., Zalc, B., Thomas, J. L., Guillemot, F., Nait-Oumesmar, B. and Parras, C. 2013. Ascl1/mash1 promotes brain oligodendrogenesis during myelination and remyelination. J. Neurosci. 33, 9752-9768.   DOI
21 Nguyen, H. T. N., Kato, H., Masuda, K., Yamaza, H., Hirofuji, Y., Sato, H., Pham, T. T. M., Takayama, F., Sakai, Y., Ohga, S., Taguchi, T. and Nonaka, K. 2018. Impaired neurite development associated with mitochondrial dysfunction in dopaminergic neurons differentiated from exfoliated deciduous tooth-derived pulp stem cells of children with autism spectrum disorder. Biochem. Biophys. Rep. 16, 24-31.
22 Parras, C. M., Galli, R., Britz, O., Soares, S., Galichet, C., Battiste, J., Johnson, J. E., Nakafuku, M., Vescovi, A. and Guillemot, F. 2004. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495-4505.   DOI
23 Ray, S., Corenblum, M. J., Anandhan, A., Reed, A., Ortiz, F. O., Zhang, D. D., Barnes, C. A. and Madhavan, L. 2018. A role for nrf2 expression in defining the aging of hippocampal neural stem cells. Cell Transplant. 27, 589-606.   DOI
24 Bertrand, N., Castro, D. S. and Guillemot, F. 2002. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.   DOI
25 Cabello-Rivera, D., Sarmiento-Soto, H., Lopez-Barneo, J. and Munoz-Cabello, A. M. 2019. Mitochondrial complex i function is essential for neural stem/progenitor cells proliferation and differentiation. Front. Neurosci. 13, 664.   DOI
26 Cabezas, R., Avila, M. F., Gonzalez, J., El-Bacha, R. S. and Barreto, G. E. 2015. Pdgf-bb protects mitochondria from rotenone in t98g cells. Neurotox. Res. 27, 355-367.   DOI
27 Pistollato, F., Canovas-Jorda, D., Zagoura, D. and Bal-Price, A. 2017. Nrf2 pathway activation upon rotenone treatment in human ipsc-derived neural stem cells undergoing differentiation towards neurons and astrocytes. Neurochem. Int. 108, 457-471.   DOI