[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.5483/BMBRep.2013.46.8.164

Interplay between autophagy and programmed cell death in mammalian neural stem cells

Chung, Kyung Min (Department of Brain Science, Daegu Gyeongbuk Institute of Science and Technology)
Yu, Seong-Woon (Department of Brain Science, Daegu Gyeongbuk Institute of Science and Technology)

Publication Information

BMB Reports / v.46, no.8, 2013 , pp. 383-390 More about this Journal

Abstract

Mammalian neural stem cells (NSCs) are of particular interest because of their role in brain development and function. Recent findings suggest the intimate involvement of programmed cell death (PCD) in the turnover of NSCs. However, the underlying mechanisms of PCD are largely unknown. Although apoptosis is the best-defined form of PCD, accumulating evidence has revealed a wide spectrum of PCD encompassing apoptosis, autophagic cell death (ACD) and necrosis. This mini-review aims to illustrate a unique regulation of PCD in NSCs. The results of our recent studies on autophagic death of adult hippocampal neural stem (HCN) cells are also discussed. HCN cell death following insulin withdrawal clearly provides a reliable model that can be used to analyze the molecular mechanisms of ACD in the larger context of PCD. More research efforts are needed to increase our understanding of the molecular basis of NSC turnover under degenerating conditions, such as aging, stress and neurological diseases. Efforts aimed at protecting and harnessing endogenous NSCs will offer novel opportunities for the development of new therapeutic strategies for neuropathologies.

Keywords

Autophagic cell death; Neural stem cells; Neurodegeneration; Programmed cell death;

Citations & Related Records

Times Cited By KSCI : 2 (Citation Analysis)

Reference
Cited By KSCI

1	Cui, X. P., Xing, Y., Chen, J. M., Dong, S. W., Ying, D. J. and Yew, D. T. (2011) Wnt/beta-catenin is involved in the proliferation of hippocampal neural stem cells induced by hypoxia. Ir. J. Med. Sci. 180, 387-393. DOI ScienceOn
2	Mazumdar, J., O'Brien, W. T., Johnson, R. S., LaManna, J. C., Chavez, J. C., Klein, P. S. and Simon, M. C. (2010) O2 regulates stem cells through Wnt/beta-catenin signalling. Nat. Cell Biol. 12, 1007-1013. DOI ScienceOn
3	Muroyama, Y., Kondoh, H. and Takada, S. (2004) Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem. Biophys. Res. Commun. 313, 915-921. DOI ScienceOn
4	Biebl, M., Cooper, C. M., Winkler, J. and Kuhn, H. G. (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett. 291, 17-20. DOI ScienceOn
5	de la Rosa, E. J. and de Pablo, F. (2000) Cell death in early neural development: beyond the neurotrophic theory. Trends Neurosci. 23, 454-458. DOI ScienceOn
6	Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A. and Gage, F. H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. DOI ScienceOn
7	Morshead, C. M. and van der Kooy, D. (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 12, 249-256.
8	Fernando, P., Brunette, S. and Megeney, L. A. (2005) Neural stem cell differentiation is dependent upon endogenous caspase 3 activity. FASEB J. 19, 1671-1673.
9	Jeon, S. M., Cheon, S. M., Bae, H. R., Kim, J. W. and Kim, S. U. (2010) Selective susceptibility of human dopaminergic neural stem cells to dopamine-induced apoptosis. Exp. Neurobiol. 19, 155-164. DOI ScienceOn
10	Han, S. I., Kim, Y. S. and Kim, T. H. (2008) Role of apoptotic and necrotic cell death under physiologic conditions. BMB Rep. 41, 1-10. 과학기술학회마을 DOI ScienceOn
11	Ha, H. C. and Snyder, S. H. (1999) Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. U. S. A. 96, 13978-13982. DOI ScienceOn
12	Maiuri, M. C., Le Toumelin, G., Criollo, A., Rain, J. C., Gautier, F., Juin, P., Tasdemir, E., Pierron, G., Troulinaki, K., Tavernarakis, N., Hickman, J. A., Geneste, O. and Kroemer, G. (2007) Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 26, 2527-2539. DOI ScienceOn
13	Yu, L., Alva, A., Su, H., Dutt, P., Freundt, E., Welsh, S., Baehrecke, E. H. and Lenardo, M. J. (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500-1502. DOI ScienceOn
14	Zalckvar, E., Yosef, N., Reef, S., Ber, Y., Rubinstein, A. D., Mor, I., Sharan, R., Ruppin, E. and Kimchi, A. (2010) A systems level strategy for analyzing the cell death network: implication in exploring the apoptosis/autophagy connection. Cell Death Differ. 17, 1244-1253. DOI ScienceOn
15	Luo, S. and Rubinsztein, D. C. (2010) Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL. Cell Death Differ. 17, 268-277. DOI ScienceOn
16	Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D. and Levine, B. (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939. DOI ScienceOn
17	Erecinska, M. and Silver, I. A. (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir. Physiol. 128, 263-276. DOI ScienceOn
18	Akanda, N., Tofighi, R., Brask, J., Tamm, C., Elinder, F. and Ceccatelli, S. (2008) Voltage-dependent anion channels (VDAC) in the plasma membrane play a critical role in apoptosis in differentiated hippocampal neurons but not in neural stem cells. Cell Cycle 7, 3225-3234. DOI
19	Holowacz, T., Huelsken, J., Dufort, D. and van der Kooy, D. (2011) Neural stem cells are increased after loss of beta-catenin, but neural progenitors undergo cell death. Eur. J. Neurosci. 33, 1366-1375. DOI ScienceOn
20	Shi, J., Parada, L. F. and Kernie, S. G. (2005) Bax limits adult neural stem cell persistence through caspase and IP3 receptor activation. Cell Death Differ. 12, 1601-1612. DOI ScienceOn
21	Mohyeldin, A., Garzon-Muvdi, T. and Quinones-Hinojosa, A. (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem. Cell 7, 150-161. DOI ScienceOn
22	Lindsten, T., Golden, J. A., Zong, W. X., Minarcik, J., Harris, M. H. and Thompson, C. B. (2003) The proapoptotic activities of Bax and Bak limit the size of the neural stem cell pool. J. Neurosci. 23, 11112-11119.
23	Raoul, C., Henderson, C. E. and Pettmann, B. (1999) Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J. Cell Biol. 147, 1049-1062. DOI ScienceOn
24	Lee, E. W., Seo, J., Jeong, M., Lee, S. and Song, J. (2012) The roles of FADD in extrinsic apoptosis and necroptosis. BMB Rep. 45, 496-508. 과학기술학회마을 DOI ScienceOn
25	Ceccatelli, S., Tamm, C., Sleeper, E. and Orrenius, S. (2004) Neural stem cells and cell death. Toxicol. Lett. 149, 59-66. DOI ScienceOn
26	Knight, J. C., Scharf, E. L. and Mao-Draayer, Y. (2010) Fas activation increases neural progenitor cell survival. J. Neurosci. Res. 88, 746-757.
27	Boya, P., Gonzalez-Polo, R. A., Casares, N., Perfettini, J. L., Dessen, P., Larochette, N., Metivier, D., Meley, D., Souquere, S., Yoshimori, T., Pierron, G., Codogno, P. and Kroemer, G. (2005) Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25, 1025-1040. DOI ScienceOn
28	Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111.
29	Kourtis, N. and Tavernarakis, N. (2009) Autophagy and cell death in model organisms. Cell Death Differ. 16, 21-30. DOI ScienceOn
30	Fimia, G. M. and Piacentini, M. (2010) Regulation of autophagy in mammals and its interplay with apoptosis. Cell. Mol. Life Sci. 67, 1581-1588. DOI
31	Kroemer, G. and Levine, B. (2008) Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 9, 1004-1010. DOI ScienceOn
32	Clarke, P. G. and Puyal, J. (2012) Autophagic cell death exists. Autophagy 8, 867-869. DOI
33	Shen, H. M. and Codogno, P. (2011) Autophagic cell death: Loch Ness monster or endangered species? Autophagy 7, 457-465. DOI ScienceOn
34	Uchiyama, Y., Koike, M., Shibata, M. and Sasaki, M. (2009) Autophagic neuron death. Methods Enzymol. 453, 33-51. DOI ScienceOn
35	Machida, M., Fujimaki, S., Hidaka, R., Asashima, M. and Kuwabara, T. (2012) The insulin regulatory network in adult hippocampus and pancreatic endocrine system. Stem Cells Int. 2012, 959737.
36	Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M. and Kroemer, G. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446. DOI ScienceOn
37	Vahsen, N., Cande, C., Briere, J. J., Benit, P., Joza, N., Larochette, N., Mastroberardino, P. G., Pequignot, M. O., Casares, N., Lazar, V., Feraud, O., Debili, N., Wissing, S., Engelhardt, S., Madeo, F., Piacentini, M., Penninger, J. M., Schagger, H., Rustin, P. and Kroemer, G. (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J. 23, 4679-4689. DOI ScienceOn
38	Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S. and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489. DOI ScienceOn
39	Bortner, C. D., Hughes, F. M. Jr. and Cidlowski, J. A. (1997) A primary role for K+ and Na+ efflux in the activation of apoptosis. J. Biol. Chem. 272, 32436-32442. DOI ScienceOn
40	Zhu, C., Qiu, L., Wang, X., Hallin, U., Cande, C., Kroemer, G., Hagberg, H. and Blomgren, K. (2003) Involvement of apoptosis-inducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain. J. Neurochem. 86, 306-317.
41	Yu, S. W., Wang, H., Poitras, M. F., Coombs, C., Bowers, W. J., Federoff, H. J., Poirier, G. G., Dawson, T. M. and Dawson, V. L. (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297, 259-263. DOI ScienceOn
42	Sun, Y., Zhang, Y., Wang, X., Blomgren, K. and Zhu, C. (2012) Apoptosis-inducing factor downregulation increased neuronal progenitor, but not stem cell, survival in the neonatal hippocampus after cerebral hypoxiaischemia. Mol. Neurodegener. 7, 17. DOI
43	Clarke, L. and van der Kooy, D. (2009) Low oxygen enhances primitive and definitive neural stem cell colony formation by inhibiting distinct cell death pathways. Stem Cells 27, 1879-1886. DOI ScienceOn
44	Morrison, R. S., Kinoshita, Y., Johnson, M. D., Guo, W. and Garden, G. A. (2003) p53-dependent cell death signaling in neurons. Neurochem. Res. 28, 15-27. DOI ScienceOn
45	Gage, F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438. DOI ScienceOn
46	Tamm, C., Zhivotovsky, B. and Ceccatelli, S. (2008) Caspase-2 activation in neural stem cells undergoing oxidative stress-induced apoptosis. Apoptosis 13, 354-363. DOI
47	Danial, N. N. and Korsmeyer, S. J. (2004) Cell death: critical control points. Cell 116, 205-219. DOI ScienceOn
48	Lockshin, R. A. and Williams, C. M. (1965) Programmed Cell Death--I. Cytology of Degeneration in the Intersegmental Muscles of the Pernyi Silkmoth. J. Insect. Physiol. 11, 123-133. DOI ScienceOn
49	Baehrecke, E. H. (2005) Autophagy: dual roles in life and death? Nat. Rev. Mol. Cell Biol. 6, 505-510. DOI ScienceOn
50	Clarke, P. G. (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl) 181, 195-213.
51	Galluzzi, L., Maiuri, M. C., Vitale, I., Zischka, H., Castedo, M., Zitvogel, L. and Kroemer, G. (2007) Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 14, 1237-1243. DOI ScienceOn
52	Shintani, T. and Klionsky, D. J. (2004) Autophagy in health and disease: a double-edged sword. Science 306, 990-995. DOI ScienceOn
53	Gozuacik, D. and Kimchi, A. (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23, 2891-2906. DOI ScienceOn
54	Kerr, J. F., Wyllie, A. H. and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257. DOI ScienceOn
55	Yuan, J. (2006) Divergence from a dedicated cellular suicide mechanism: exploring the evolution of cell death. Mol. Cell 23, 1-12. DOI ScienceOn
56	Wajant, H. (2003) Death receptors. Essays Biochem. 39, 53-71. DOI
57	Meletis, K., Wirta, V., Hede, S. M., Nister, M., Lundeberg, J. and Frisen, J. (2006) p53 suppresses the self-renewal of adult neural stem cells. Development 133, 363-369.
58	Li, J. and Yuan, J. (2008) Caspases in apoptosis and beyond. Oncogene 27, 6194-6206. DOI ScienceOn
59	Meijer, A. J. and Codogno, P. (2004) Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36, 2445-2462. DOI ScienceOn
60	Pospisilik, J. A., Knauf, C., Joza, N., Benit, P., Orthofer, M., Cani, P. D., Ebersberger, I., Nakashima, T., Sarao, R., Neely, G., Esterbauer, H., Kozlov, A., Kahn, C. R., Kroemer, G., Rustin, P., Burcelin, R. and Penninger, J. M. (2007) Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131, 476-491. DOI ScienceOn
61	Shen, S., Kepp, O. and Kroemer, G. (2012) The end of autophagic cell death? Autophagy 8, 1-3. DOI ScienceOn
62	Romanko, M. J., Rothstein, R. P. and Levison, S. W. (2004) Neural stem cells in the subventricular zone are resilient to hypoxia/ischemia whereas progenitors are vulnerable. J. Cereb. Blood Flow Metab. 24, 814-825. DOI ScienceOn
63	Yu, S. W., Baek, S. H., Brennan, R. T., Bradley, C. J., Park, S. K., Lee, Y. S., Jun, E. J., Lookingland, K. J., Kim, E. K., Lee, H., Goudreau, J. L. and Kim, S. W. (2008) Autophagic death of adult hippocampal neural stem cells following insulin withdrawal. Stem Cells 26, 2602-2610. DOI ScienceOn
64	Koike, M., Shibata, M., Tadakoshi, M., Gotoh, K., Komatsu, M., Waguri, S., Kawahara, N., Kuida, K., Nagata, S., Kominami, E., Tanaka, K. and Uchiyama, Y. (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am. J. Pathol. 172, 454-469. DOI ScienceOn
65	Sun, W., Winseck, A., Vinsant, S., Park, O. H., Kim, H. and Oppenheim, R. W. (2004) Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J. Neurosci. 24, 11205-11213. DOI ScienceOn
66	Yadirgi, G., Leinster, V., Acquati, S., Bhagat, H., Shakhova, O. and Marino, S. (2011) Conditional activation of Bmi1 expression regulates self-renewal, apoptosis, and differentiation of neural stem/progenitor cells in vitro and in vivo. Stem Cells 29, 700-712. DOI ScienceOn
67	Shetty, G. A., Hattiangady, B. and Shetty, A. K. (2013) Neural stem cell- and neurogenesis-related gene expression profiles in the young and aged dentate gyrus. Age (Dordr). (In press).
68	Agrawal, S. and Schaffer, D. V. (2005) In situ stem cell therapy: novel targets, familiar challenges. Trends Biotechnol. 23, 78-83. DOI ScienceOn

11	Linda Ingemann. (2014) Journal of Lipid Research Lysosomal storage diseases and the heat shock response: convergences and therapeutic opportunities / 55 (11) , 2198
	Kyung Min Chung. (2016) Frontiers in Cellular Neuroscience Mediation of Autophagic Cell Death by Type 3 Ryanodine Receptor (RyR3) in Adult Hippocampal Neural Stem Cells / 10
5	Hye Park. (2014) Molecules Fucoidan Inhibits the Proliferation of Human Urinary Bladder Cancer T24 Cells by Blocking Cell Cycle Progression and Inducing Apoptosis / 19 (5) , 5981
1	Xue-Yu Fan. (2015) Scientific Reports Activation of the AMPK-ULK1 pathway plays an important role in autophagy during prion infection / 5 (1)
1	Bruno S. F. Souza. (2016) Scientific Reports Zika virus infection induces mitosis abnormalities and apoptotic cell death of human neural progenitor cells / 6 (1)
	Caroline Jeeyeon Hong. (2016) Brain Research Autophagy for the quality control of adult hippocampal neural stem cells / 1649 , 166
33	Shinwon Ha. (2017) Journal of Biological Chemistry Phosphorylation of p62 by AMP-activated protein kinase mediates autophagic cell death in adult hippocampal neural stem cells / 292 (33) , 13795
4	GUK HEUI JO. (2014) International Journal of Oncology Sulforaphane induces apoptosis in T24 human urinary bladder cancer cells through a reactive oxygen species-mediated mitochondrial pathway: The involvement of endoplasmic reticulum stress and the Nrf2 signaling pathway / 45 (4) , 1497
1	Shinwon Ha. (2015) Molecular Brain Regulation of autophagic cell death by glycogen synthase kinase-3β in adult hippocampal neural stem cells following insulin withdrawal / 8 (1)
3	Jae-Sun Shin. (2014) Biochemical and Biophysical Research Communications Targeting of p53 peptide analogues to anti-apoptotic Bcl-2 family proteins as revealed by NMR spectroscopy / 443 (3) , 882
9	(2017) Cell Transplantation Oxidative Stress in Stem Cell Aging / 26 (9) , 1483
1432-0878	(2018) Cell and Tissue Research Roles of autophagy in controlling stem cell identity: a perspective of self-renewal and differentiation / (1432-0878)
1554-8635	(2019) Autophagy Vitamin D improves sunburns by increasing autophagy in M2 macrophages / (1554-8635) , 1
6	(2014) Oncology Reports Induction of apoptosis in MDA-MB-231 human breast carcinoma cells with an ethanol extract of Cyperus rotundus L. by activating caspases / 32 (6) , 2461
1	(2018) Molecular Brain Chronic restraint stress induces hippocampal memory deficits by impairing insulin signaling / 11 (1)