The differential DRP1 phosphorylation and mitochondrial dynamics in the regional specific astroglial death induced by status Epilepticus

Frontiers in Cellular Neuroscience

Volumn 10, Issue MAY, 2016, Pages

  Ko, Ah Reum ^a   Hyun, Hye Won ^a   Min, Su Ji ^a   Kim, Ji Eun ^a  

^a Hallym University   (South Korea)

Author keywords

Astroglial death; Clasmatodendrosis; DRP1; Mitochondria; Status epilepticus

Indexed keywords

ATROPINE METHYL BROMIDE; DIAZEPAM; DYNAMIN-RELATED PROTEIN 1; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GUANOSINE TRIPHOSPHATASE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MDIVI-1; PILOCARPINE; PIRINIXIC ACID; RINGER LACTATE SOLUTION; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; CELL COUNT; CELL DEATH; CONFOCAL LASER SCANNING MICROSCOPE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MACROGLIA; MALE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FISSION; MITOCHONDRIAL LENGTH; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT;

EID: 84969263241     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2016.00124     Document Type: Article

References (72)

1. Alaimo, A., Gorojod, R. M., Beauquis, J., Muñoz, M. J., Saravia, F., and Kotler, M. L. (2014). Deregulation of mitochondria-shaping proteins Opa-1 and Drp-1 in manganese-induced apoptosis. PLoS One 9:e91848. doi: 10.1371/journal.pone.0091848
2. Anderson, C. M., and Swanson, R. A. (2000). Astrocyte glutamate transport: review of properties, regulation and physiological functions. Glia 32, 1-14. doi: 10.1002/1098-1136(200010)32:1<1::aid-glia10>3.3.co;2-n
3. Bach, D., Pich, S., Soriano, F. X., Vega, N., Baumgartner, B., Oriola, J., et al. (2003). Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278, 17190-17197. doi: 10.1074/jbc.m212754200
4. Benard, G., and Rossignol, R. (2008). Ultrastructure of the mitochondrion and its bearing on function and bioenergetics. Antioxid. Redox Signal. 10, 1313-1342. doi: 10.1089/ars.2007.2000
5. Birsa, N., Norkett, R., Higgs, N., Lopez-Domenech, G., and Kittler, J. T. (2013). Mitochondrial trafficking in neurons and the role of the miro family of GTPase proteins. Biochem. Soc. Trans. 41, 1525-1531. doi: 10.1042/BST20130234
6. Bordey, A., and Sontheimer, H. (1998). Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res. 32, 286-303. doi: 10.1016/s0920-1211(98)00059-x
7. Borges, K., McDermott, D., Irier, H., Smith, Y., and Dingledine, R. (2006). Degeneration and proliferation of astrocytes in the mouse dentate gyrus after pilocarpine-induced status epilepticus. Exp. Neurol. 201, 416-427. doi: 10.1016/j.expneurol.2006.04.031
8. Campello, S., and Scorrano, L. (2010). Mitochondrial shape changes: orchestrating cell pathophysiology. EMBO Rep. 11, 678-684. doi: 10.1038/embor.2010.115
9. Cassidy-Stone, A., Chipuk, J. E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., et al. (2008). Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14, 193-204. doi: 10.1016/j.devcel.2007.11.019
10. Chen, H., and Chan, D. C. (2005). Emerging functions of mammalian mitochondrial fusion and fission. Hum. Mol. Genet. 14, R283-R289. doi: 10.1093/hmg/ddi270
11. Chen, H., and Chan, D. C. (2009). Mitochondrial dynamics-fusion, fission, movement and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18, R169-R176. doi: 10.1093/hmg/ddp326
12. Chen, H., Chomyn, A., and Chan, D. C. (2005). Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185-26192. doi: 10.1074/jbc.m503062200
13. Chen, H., Detmer, S. A., Ewald, A. J., Griffin, E. E., Fraser, S. E., and Chan, D. C. (2003). Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189-200. doi: 10.1083/jcb.200211046
14. Chen, Y., McMillan-Ward, E., Kong, J., Israels, S. J., and Gibson, S. B. (2007). Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J. Cell Sci. 120, 4155-4166. doi: 10.1242/jcs.011163
15. Cheung, E. C., McBride, H. M., and Slack, R. S. (2007). Mitochondrial dynamics in the regulation of neuronal cell death. Apoptosis 12, 979-992. doi: 10.1007/s10495-007-0745-5
16. Cipolat, S., Martins de Brito, O., Dal Zilio, B., and Scorrano, L. (2004). OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U S A 101, 15927-15932. doi: 10.1073/pnas.0407043101
17. Deloncle, R., Huguet, F., Fernandez, B., Quellard, N., Babin, P., and Guillard, O. (2001). Ultrastructural study of rat hippocampus after chronic administration of aluminum L-glutamate: an acceleration of the aging process. Exp. Gerontol. 36, 231-244. doi: 10.1016/s0531-5565(00)00214-x
18. Detmer, S. A., and Chan, D. C. (2007). Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8, 870-879. doi: 10.1038/nrm2275
19. Dihné, M., Block, F., Korr, H., and Töpper, R. (2001). Time course of glial proliferation and glial apoptosis following excitotoxic CNS injury. Brain Res. 902, 178-189. doi: 10.1016/s0006-8993(01)02378-2
20. DuBoff, B., Götz, J., and Feany, M. B. (2012). Tau promotes neurodegeneration via DRP1 mislocalization in vivo. Neuron 75, 618-632. doi: 10.1016/j.neuron.2012.06.026
21. Friede, R. L., and van Houten, W. H. (1961). Relations between postmortem alterations and glycolytic metabolism in the brain. Exp. Neurol. 4, 197-204. doi: 10.1016/0014-4886(61)90041-3
22. Greene, J. G., Borges, K., and Dingledine, R. (2009). Quantitative transcriptional neuroanatomy of the rat hippocampus: evidence for wide-ranging, pathway-specific heterogeneity among three principal cell layers. Hippocampus 19, 253-264. doi: 10.1002/hipo.20502
23. Gualtieri, F., Curia, G., Marinelli, C., and Biagini, G. (2012). Increased perivascular laminin predicts damage to astrocytes in CA3 and piriform cortex following chemoconvulsive treatments. Neuroscience 218, 278-294. doi: 10.1016/j.neuroscience.2012.05.018
24. Horn, S. R., Thomenius, M. J., Johnson, E. S., Freel, C. D., Wu, J. Q., Coloff, J. L., et al. (2011). Regulation of mitochondrial morphology by APC/CCdh1-mediated control of Drp1 stability. Mol. Biol. Cell 22, 1207-1216. doi: 10.1091/mbc.e10-07-0567
25. Hulse, R. E., Winterfield, J., Kunkler, P. E., and Kraig, R. P. (2001). Astrocytic clasmatodendrosis in hippocampal organ culture. Glia 33, 169-179. doi: 10.1002/1098-1136(200102)33:23.0.CO;2-B
26. Ingvar, M., Schmidt-Kastner, R., and Meller, D. (1994). Immunohistochemical markers for neurons and astrocytes show pan-necrosis following infusion of high-dose NMDA into rat cortex. Exp. Neurol. 128, 249-259. doi: 10.1006/exnr.1994.1134
27. Jahani-Asl, A., Cheung, E. C., Neuspiel, M., MacLaurin, J. G., Fortin, A., Park, D. S., et al. (2007). Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J. Biol. Chem. 282, 23788-23798. doi: 10.1074/jbc.m703812200
28. Ju, W. K., Kim, K. Y., Noh, Y. H., Hoshijima, M., Lukas, T. J., Ellisman, M. H., et al. (2015). Increased mitochondrial fission and volume density by blocking glutamate excitotoxicity protect glaucomatous optic nerve head astrocytes. Glia 63, 736-753. doi: 10.1002/glia.22781
29. Kageyama, Y., Zhang, Z., Roda, R., Fukaya, M., Wakabayashi, J., Wakabayashi, N., et al. (2012). Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J. Cell Biol. 197, 535-551. doi: 10.1083/jcb.201110034
30. Kang, T. C., Kim, D. S., Kwak, S. E., Kim, J. E., Won, M. H., Kim, D. W., et al. (2006). Epileptogenic roles of astroglial death and regeneration in the dentate gyrus of experimental temporal lobe epilepsy. Glia 54, 258-271. doi: 10.1002/glia.20380
31. Kashatus, D. F., Lim, K. H., Brady, D. C., Pershing, N. L., Cox, A. D., and Counter, C. M. (2011). RALA and RALBP1 regulate mitochondrial fission at mitosis. Nat. Cell Biol. 13, 1108-1115. doi: 10.1038/ncb2310
32. Kim, J. E., Kim, Y. J., Kim, J. Y., and Kang, T. C. (2014a). PARP1 activation/expression modulates regional-specific neuronal and glial responses to seizure in a hemodynamic-independent manner. Cell Death Dis. 5:e1362. doi: 10.1038/cddis.2014.331
33. Kim, J. E., Ryu, H. J., Kim, M. J., and Kang, T. C. (2014b). LIM kinase-2 induces programmed necrotic neuronal death via dysfunction of DRP1-mediated mitochondrial fission. Cell Death Differ. 21, 1036-1049. doi: 10.1038/cdd.2014.17
34. Kim, D. S., Kim, J. E., Kwak, S. E., Choi, K. C., Kim, D. W., Kwon, O. S., et al. (2008). Spatiotemporal characteristics of astroglial death in the rat hippocampo-entorhinal complex following pilocarpine-induced status epilepticus. J. Comp. Neurol. 511, 581-598. doi: 10.1002/cne.21851
35. Kim, J. E., Ryu, H. J., and Kang, T. C. (2013). Status epilepticus induces vasogenic edema via tumor necrosis factor-α /endothelin-1-mediated two different pathways. PLoS One 8:e74458. doi: 10.1371/journal.pone.0074458
36. Kim, J. E., Ryu, H. J., Kim, M. J., Kim, D. W., Kwon, O. S., Choi, S. Y., et al. (2010a). Pyridoxal-5’-phosphate phosphatase/chronophin induces astroglial apoptosis via actin-depolymerizing factor/cofilin system in the rat brain following status epilepticus. Glia 58, 1937-1948. doi: 10.1002/glia.21063
37. Kim, J. E., Yeo, S. I., Ryu, H. J., Kim, M. J., Kim, D. S., Jo, S. M., et al. (2010b). Astroglial loss and edema formation in the rat piriform cortex and hippocampus following pilocarpine-induced status epilepticus. J. Comp. Neurol. 518, 4612-4628. doi: 10.1002/cne.22482
38. Kim, J. E., Ryu, H. J., Yeo, S. I., and Kang, T. C. (2011). P2X7 receptor differentially modulates astroglial apoptosis and clasmatodendrosis in the rat brain following status epilepticus. Hippocampus 21, 1318-1333. doi: 10.1002/hipo.20850
39. Kim, J. E., Ryu, H. J., Yeo, S. I., Seo, C. H., Lee, B. C., Choi, I. G., et al. (2009). Differential expressions of aquaporin subtypes in astroglia in the hippocampus of chronic epileptic rats. Neuroscience 163, 781-789. doi: 10.1016/j.neuroscience.2009.07.028
40. Kraig, R. P., and Chesler, M. (1990). Astrocytic acidosis in hyperglycemic and complete ischemia. J. Cereb. Blood Flow Metab. 10, 104-114. doi: 10.1038/jcbfm.1990.13
41. Lee, M. C., Ting, K. K., Adams, S., Brew, B. J., Chung, R., and Guillemin, G. J. (2010). Characterisation of the expression of NMDA receptors in human astrocytes. PLoS One 5:e14123. doi: 10.1371/journal.pone.0014123
42. Li, Z., Okamoto, K., Hayashi, Y., and Sheng, M. (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887. doi: 10.1016/j.cell.2004.11.003
43. Liesa, M., Palacín, M., and Zorzano, A. (2009). Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 89, 799-845. doi: 10.1152/physrev.00030.2008
44. Lin, C. J., Chen, T. H., Yang, L. Y., and Shih, C. M. (2014). Resveratrol protects astrocytes against traumatic brain injury through inhibiting apoptotic and autophagic cell death. Cell Death Dis. 5:e1147. doi: 10.1038/cddis.2014.123
45. Lundgren, B., Bergstrand, A., Karlsson, K., and DePierre, J. W. (1990). Effects of dietary treatment with clofibrate, nafenopin or WY-14.643 on mitochondria and DNA in mouse liver. Biochim. Biophys. Acta 1035, 132-138. doi: 10.1016/0304-4165(90)90107-8
46. MacAskill, A. F., Atkin, T. A., and Kittler, J. T. (2010). Mitochondrial trafficking and the provision of energy and calcium buffering at excitatory synapses. Eur. J. Neurosci. 32, 231-240. doi: 10.1111/j.1460-9568.2010.07345.x
47. Mathern, G. W., Pretorius, J. K., Kornblum, H. I., Mendoza, D., Lozada, A., Leite, J. P., et al. (1998). Altered hippocampal kainate-receptor mRNA levels in temporal lobe epilepsy patients. Neurobiol. Dis. 5, 151-176. doi: 10.1006/nbdi.1998.0200
48. Olichon, A., Baricault, L., Gas, N., Guillou, E., Valette, A., Belenguer, P., et al. (2003). Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278, 7743-7746. doi: 10.1074/jbc.c200677200
49. Parone, P. A., Da Cruz, S., Tondera, D., Mattenberger, Y., James, D. I., Maechler, P., et al. (2008). Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 3:e3257. doi: 10.1371/journal.pone.0003257
50. Penfield, W. (1928). ‘Neuroglia and microglia-the interstitial tissue of the central nervous system,’ in Special Cytology, the Form and Function of the Cell in Health and Disease, ed. E. V. Cowdry (New York, NY: Hoeber), 1033-1068.
51. Rambold, A. S., Kostelecky, B., Elia, N., and Lippincott-Schwartz, J. (2011). Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. U S A 108, 10190-10195. doi: 10.1073/pnas.1107402108
52. Ransom, B., Behar, T., and Nedergaard, M. (2003). New roles for astrocytes (stars at last). Trends Neurosci. 26, 520-522. doi: 10.1016/j.tins.2003.08.006
53. Revuelta, M., Castaño, A., Machado, A., Cano, J., and Venero, J. L. (2005). Kainate-induced zinc translocation from presynaptic terminals causes neuronal and astroglial cell death and mRNA loss of BDNF receptors in the hippocampal formation and amygdala. J. Neurosci. Res. 82, 184-195. doi: 10.1002/jnr.20632
54. Rintoul, G. L., and Reynolds, I. J. (2010). Mitochondrial trafficking and morphology in neuronal injury. Biochim. Biophys. Acta 1802, 143-150. doi: 10.1016/j.bbadis.2009.09.005
55. Rolland, S. G., Motori, E., Memar, N., Hench, J., Frank, S., Winklhofer, K. F., et al. (2013). Impaired complex IV activity in response to loss of LRPPRC function can be compensated by mitochondrial hyperfusion. Proc. Natl. Acad. Sci. U S A 110, E2967-E2976. doi: 10.1073/pnas.1303872110
56. Ryu, H. J., Kim, J. E., Yeo, S. I., and Kang, T. C. (2011a). p65/RelA-Ser529 NF-κB subunit phosphorylation induces autophagic astroglial death (Clasmatodendrosis) following status epilepticus. Cell Mol. Neurobiol. 31, 1071-1078. doi: 10.1007/s10571-011-9706-1
57. Ryu, H. J., Kim, J. E., Yeo, S. I., Kim, D. W., Kwon, O. S., Choi, S. Y., et al. (2011b). F-actin depolymerization accelerates clasmatodendrosis via activation of lysosome-derived autophagic astroglial death. Brain Res. Bull. 85, 368-373. doi: 10.1016/j.brainresbull.2011.05.007
58. Schmidt-Kastner, R., and Ingvar, M. (1994). Loss of immunoreactivity for glial fibrillary acidic protein (GFAP) in astrocytes as a marker for profound tissue damage in substantia nigra and basal cortical areas after status epilepticus induced by pilocarpine in rat. Glia 12, 165-172. doi: 10.1002/glia.440120302
59. Schmidt-Kastner, R., and Ingvar, M. (1996). Laminar damage of neurons and astrocytes in neocortex and hippocampus of rat after long-lasting status epilepticus induced by pilocarpine. Epilepsy Res. Suppl. 12, 309-316.
60. Sheng, Z. H., and Cai, Q. (2012). Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 13, 77-93. doi: 10.1038/nrn3156
61. Smirnova, E., Griparic, L., Shurland, D. L., and van der Bliek, A. M. (2001). Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256. doi: 10.1091/mbc.12.8.2245
62. Sugawara, T., Lewén, A., Noshita, N., Gasche, Y., and Chan, P. H. (2002). Effects of global ischemia duration on neuronal, astroglial, oligodendroglial and microglial reactions in the vulnerable hippocampal CA1 subregion in rats. J. Neurotrauma 19, 85-98. doi: 10.1089/089771502753460268
63. Sung, J. Y., Engmann, O., Teylan, M. A., Nairn, A. C., Greengard, P., and Kim, Y. (2008). WAVE1 controls neuronal activity-induced mitochondrial distribution in dendritic spines. Proc. Natl. Acad. Sci. U S A 105, 3112-3116. doi: 10.1073/pnas.0712180105
64. Szydlowska, K., Zawadzka, M., and Kaminska, B. (2006). Neuroprotectant FK506 inhibits glutamate-induced apoptosis of astrocytes in vitro and in vivo. J. Neurochem. 99, 965-975. doi: 10.1111/j.1471-4159.2006.04136.x
65. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., and Mihara, K. (2007). Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282, 11521-11529. doi: 10.1074/jbc.m607279200
66. Tomimoto, H., Akiguchi, I., Wakita, H., Suenaga, T., Nakamura, S., and Kimura, J. (1997). Regressive changes of astroglia in white matter lesions in cerebrovascular disease and Alzheimer’s disease patients. Acta Neuropathol. 94, 146-152. doi: 10.1007/s004010050686
67. Turski, L., Ikonomidou, C., Turski, W. A., Bortolotto, Z. A., and Cavalheiro, E. A. (1989). Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 3, 154-171. doi: 10.1002/syn.890030207
68. Walker, M. C., White, H. S., and Sander, J. W. (2002). Disease modification in partial epilepsy. Brain 125, 1937-1950. doi: 10.1093/brain/awf203
69. Wang, Z., Jiang, H., Chen, S., Du, F., and Wang, X. (2012). The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148, 228-243. doi: 10.1016/j.cell.2011.11.030
70. Yim, N., Ryu, S. W., Han, E. C., Yoon, J., Choi, K., and Choi, C. (2014). Mutant ubiquitin UBB+1 inducesmitochondrial fusion by destabilizing mitochondrial fission-specific proteins and confers resistance to oxidative stress-induced cell death in astrocytic cells. PLoS One 9:e99937. doi: 10.1371/journal.pone.0099937
71. Youle, R. J., and Karbowski, M. (2005). Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6, 657-663. doi: 10.1038/nrm1697
72. Zolezzi, J. M., Silva-Alvarez, C., Ordenes, D., Godoy, J. A., Carvajal, F. J., Santos, M. J., et al. (2013). Peroxisome proliferator-activated receptor (PPAR) γ and PPARα agonists modulate mitochondrial fusion-fission dynamics: relevance to reactive oxygen species (ROS)-related neurodegenerative disorders? PLoS One 8:e64019. doi: 10.1371/journal.pone.0064019