Ryanodine receptor-mediated Ca2+ release underlies iron-induced mitochondrial fission and stimulates mitochondrial Ca2+ uptake in primary hippocampal neurons

Frontiers in Molecular Neuroscience

Volumn 7, Issue MAR, 2014, Pages

  SanMartín, Carol D ^a   Paula Lima, Andrea C ^a   García, Alejandra ^a   Barattini, Pablo ^a   Hartel, Steffen ^a   Núñez, Marco T ^a   Hidalgo, Cecilia ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

Cellular redox state; Drp 1; Endoplasmic reticulum; Mitochondrial calcium; Mitochondrial network; Reactive oxygen species

Indexed keywords

REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR;

ARTICLE; CALCIUM CELL LEVEL; CELL CULTURE; CELL FRACTIONATION; CELL FUNCTION; CELLULAR PARAMETERS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; INTRACELLULAR SIGNALING; MITOCHONDRIAL DYNAMICS; NERVE CELL; NERVE CELL PLASTICITY; QUANTITATIVE ANALYSIS; WESTERN BLOTTING;

EID: 84897431689     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00013     Document Type: Article

References (68)

1. Adasme, T., Haeger, P., Paula-Lima, A. C., Espinoza, I., Casas-Alarcon, M. M., Carrasco, M. A., et al. (2011). Involvement of ryanodine receptors in neurotrophin-induced hippocampal synaptic plasticity and spatial memory formation. Proc. Natl. Acad. Sci. U.S.A. 108, 3029-3034. doi: 10.1073/pnas.1013580108.
2. Baker, K. D., Edwards, T. M., and Rickard, N. S. (2013). The role of intracellular calcium stores in synaptic plasticityand memoryconsolidation. Neurosci. Biobehav. Rev. 37,1211-1239. doi: 10.1016/j.neubiorev.2013.04.011.
3. Bardo, S., Cavazzini, M. G., and Emptage, N. (2006). The role of the endoplasmic reticulum Ca store in the plasticity of central neurons. Trends Pharmacol. Sci. 27, 78-84. doi: 10.1016/j.tips.2005.12.008.
4. Barsoum, M. J., Yuan, H., Gerencser, A. A., Liot, G., Kushnareva, Y., Graber, S., et al. (2006). Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 25, 3900-3911. doi: 10.1038/sj.emboj.7601253.
5. 2+ and redox modification of ryanodine receptor channels from rat brain cortex. J. Neurosci. 28, 9463-9472. doi: 10.1523/JNEUROSCI.2286-08.2008.
6. 2+ dependence of RyR channels from rat brain cortex. Am. J. Physiol. Cell Physiol. 293, C162-C171. doi: 10.1152/ajpcell.00518.2006.
7. Cereghetti, G. M., Stangherlin, A., Martins De Brito, O., Chang, C. R., Blackstone, C., Bernardi, P., et al. (2008). Dephosphorylation bycalcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. U.S.A. 105, 15803-15808. doi: 10.1073/pnas.0808249105.
8. Cribbs, J. T., and Strack, S. (2007). Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8, 939-944. doi: 10.1038/sj.embor. 7401062
9. Csordas, G., and Hajnoczky, G. (2009). SR/ER-mitochondrial local communication: calcium and ROS. Biochim. Biophys. Acta 1787, 1352-1362. doi: 10.1016/j.bbabio.2009.06.004.
10. Csordas, G., Renken, C., Varnai, P., Walter, L., Weaver, D., Buttle, K. F., et al. (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921. doi: 10.1083/jcb. 200604016
11. Cho, D. H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., et al. (2009). S-nitrosylation ofDrp1 mediatesbeta-amyloid-relatedmitochondrial fission and neuronal injury. Science 324, 102-105. doi: 10.1126/science.1171091.
12. 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.
13. 2+ and reactive oxygen species signaling. J. Cell Sci. 126, 2965-2978. doi: 10.1242/jcs.093609.
14. Eisner, V., Parra, V., Lavandero, S., Hidalgo, C., and Jaimovich, E. (2010). Mitochondria fine-tune the slow Ca(2+) transients induced by electrical stimulation of skeletal myotubes. Cell Calcium 48, 358-370. doi: 10.1016/j.ceca.2010. 11.001
15. Frank, S., Gaume, B., Bergmann-Leitner, E. S., Leitner, W. W., Robert, E. G., Catez, F., et al. (2001). The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525. doi: 10.1016/S1534-5807(01) 00055-7
16. Frieden, M., James, D., Castelbou, C., Danckaert, A., Martinou, J. C., and Demau-rex, N. (2004). Ca(2+) homeostasis during mitochondrial fragmentation and perinuclear clustering induced by hFis1. J. Biol. Chem. 279, 22704-22714. doi: 10.1074/jbc.M312366200M312366200.
17. 2+ transfer between sarcoplasmic reticulum subdomains and the mitochondria in heart muscle. J. Biol. Chem. 283, 32771-32780. doi: 10.1074/jbc.M803385200.
18. Han, X. J., Lu, Y. F., Li, S. A., Kaitsuka, T., Sato, Y., Tomizawa, K., et al. (2008). CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. CellBiol. 182, 573-585. doi: 10.1083/jcb.200802164.
19. Harder, Z., Zunino, R., and Mcbride, H. (2004). Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 14, 340-345. doi: 10.1016/j.cub.2004.02.004.
20. Hidalgo, C., Carrasco, M. A., Munoz, P., and Nunez, M. T. (2007).A role for reactive oxygen/nitrogen species and iron on neuronal synaptic plasticity. Antioxid. Redox Signal. 9,245-255.doi:10.1089/ars.2007.9.ft-9.
21. Hidalgo, C., and Donoso, P. (2008). Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications. Antioxid. Redox Signal. 10, 1275-1312. doi: 10.1089/ars.2007.1886.
22. 2+ release channels: cellular redox sensors? IUBMB Life 57, 315-322. doi: 10.1080/15216540500092328.
23. Hidalgo, C., and Nunez, M. T. (2007). Calcium, iron and neuronal function. IUBMB Life 59, 280-285. doi: 10.1080/15216540701222906.
24. Hom, J. R., Gewandter, J. S., Michael, L., Sheu, S. S., and Yoon, Y. (2007). Thapsigargin induces biphasic fragmentation of mitochondria through calcium-mediated mitochondrial fission and apoptosis. J. Cell. Physiol. 212, 498-508. doi: 10.1002/jcp.21051
25. Itoh, K., Nakamura, K., Iijima, M., and Sesaki, H. (2013). Mitochondrial dynamics in neurodegeneration. Trends CellBiol. 23, 64-71. doi: 10.1016/j.tcb.2012.10.006.
26. 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.
27. 2+ and stimulates oxidative metabolism in hippocampal slice cultures. J. Neurophysiol. 90, 613-621. doi: 10.1152/jn.00042.200300042.2003.
28. Karbowski, M., Neutzner, A., and Youle, R. J. (2007). The mitochondrialE3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 178,71-84. doi: 10.1083/jcb.200611064.
29. Kehrer, J. P. (2000). The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149, 43-50. doi: 10.1016/S0300-483X(00)00231-6.
30. Kemmerling, U., Munoz, P., Muller, M., Sanchez, G., Aylwin, M. L., Klann, E., et al. (2007). Calcium release by ryanodine receptors mediates hydrogen peroxide-induced activation of ERK and CREB phosphorylation in N2a cells and hippocampal neurons. Cell Calcium 41,491-502. doi: 10.1016/j.ceca.2006.10.001.
31. Kennedy, K. A., Sandiford, S. D., Skerjanc, I. S., and Li, S. S. (2012). Reactive oxygen speciesandtheneuronalfate. Cell Mol. LifeSci. 69,215-221. doi: 10.1007/s00018-011-0807-2
32. Knott, A. B., Perkins, G., Schwarzenbacher, R., and Bossy-Wetzel, E. (2008). Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 9, 505-518. doi: 10.1038/nrn2417.
33. Kuznetsov, A. V., Hermann, M., Saks, V., Hengster, P., and Margreiter, R. (2009). The cell-type specificity of mitochondrial dynamics. Int. J. Biochem. Cell Biol. 41, 1928-1939. doi: 10.1016/j.biocel.2009.03.007.
34. 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.
35. Lopez, J. R., Lyckman, A., Oddo, S., Laferla, F. M., Querfurth, H. W., and Shtifman, A. (2008). Increased intraneuronal resting [Ca2+] in adult Alzheimer's disease mice. J. Neurochem. 105, 262-271. doi: 10.1111/j.1471-4159.2007.05135.x
36. Marchesi, V. T. (2011). Alzheimer's dementia begins as a disease of small blood vessels, damaged by oxidative-induced inflammation and dysregulated amyloid metabolism: implications for early detection and therapy. FASEB J. 25, 5-13. doi: 10.1096/fj.11-0102ufm
37. Munoz, P., Humeres, A., Elgueta, C., Kirkwood, A., Hidalgo, C., and Nunez, M. T. (2011). Iron mediates N-methyl-D-aspartate receptor-dependent stimulation of calcium-induced pathways and hippocampal synaptic plasticity. J. Biol. Chem. 286, 13382-13392. doi: 10.1074/jbc.M110.213785.
38. Munoz, P., Zavala, G., Castillo, K., Aguirre, P., Hidalgo, C., and Nunez, M. T. (2006). Effect of iron on the activation of the MAPK/ERK pathway in PC12 neuroblas-tomacells. Biol. Res. 39,189-190. doi: 10.4067/S0716-97602006000100021.
39. Nunez, M. T., Urrutia, P., Mena, N., Aguirre, P., Tapia, V., and Salazar, J. (2012). Iron toxicity in neurodegeneration. Biometals 25, 761-776. doi: 10.1007/s10534-012-9523-0
40. Orth, M., and Schapira, A. H. (2001). Mitochondria and degenerative disorders. Am.J. Med. Genet. 106,27-36. doi: 10.1002/ajmg.142510.1002/ajmg.1425.
41. 2+ marks: miniature calcium signals in single mitochondria driven by ryanodine receptors. Proc. Natl. Acad. Sci. U.S.A. 99,2380-2385. doi: 10.1073/pnas.03242369999/4/2380.
42. Parra, V., Eisner, V., Chiong, M., Criollo, A., Moraga, F., Garcia, A., et al. (2008). Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc. Res. 77, 387-397. doi: 10.1093/cvr/cvm029.
43. Paula-Lima, A. C., Brito-Moreira, J., and Ferreira, S. T. (2013). Deregulation of excitatory neurotransmission underlying synapse failure in Alzheimer's disease. J. Neurochem. 126,191-202. doi: 10.1111/jnc.12304.
44. Paula-Lima, A. C., Adasme, T., SanMartin, C., Sebollela, A., Hetz, C., Carrasco, M. A., et al. (2011). Amyloid beta-peptide oligomers stimulate RyR-mediated Ca2 + release inducing mitochondrial fragmentation in hippocampal neurons and prevent RyR-mediated dendritic spine remodeling produced by BDNF. Antioxid. Redox Signal. 14, 1209-1223. doi: 10.1089/ars.2010.3287.
45. Paula-Lima, A. C., De Felice, F. G., Brito-Moreira, J., and Ferreira, S. T. (2005). Activation of GABA(A) receptors by taurine and muscimol blocks the neurotoxicity of beta-amyloid in rat hippocampal and cortical neurons. Neuropharmacology 49, 1140-1148. doi: 10.1016/j.neuropharm.2005.06.015.
46. 2+ release channels to hippocampal synaptic plasticity and spatial memory. Potential redox modulation. Antioxid. Redox Signal. doi: 10.1089/ars.2013.5796 [Epub ahead of print].
47. Pizzo, P., and Pozzan, T. (2007). Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol. 17, 511-517. doi: 10.1016/j.tcb.2007.07.011.
48. Pletjushkina, O. Y., Lyamzaev, K. G., Popova, E. N., Nepryakhina, O. K., Ivanova, O. Y., Domnina, L. V., et al. (2006). Effect of oxidative stress on dynamics of mitochondrial reticulum. Biochim. Biophys. Acta 1757, 518-524. doi: 10.1016/j.bbabio.2006.03.018.
49. Rintoul, G. L., Filiano, A. J., Brocard, J. B., Kress, G. J., and Reynolds, I. J. (2003). Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J. Neurosci. 23, 7881-7888.
50. 2+ release and generates hydrogen peroxide, which jointly stimulate NF-kappaB activity. Antioxid. Redox Signal. 14, 1245-1259. doi: 10.1089/ars.2010.3238.
51. Rizzuto, R., Simpson, A. W., Brini, M., and Pozzan, T. (1992). Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature358, 325-327. doi: 10.1038/358325a0.
52. Rusnak, F., and Mertz, P. (2000). Calcineurin: form and function. Physiol. Rev. 80, 1483-1521.
53. SanMartin, C. D., Adasme, T., Hidalgo, C., and Paula-Lima, A. C. (2012). The antioxidant N-acetylcysteine prevents the mitochondrial fragmentation induced by soluble amyloid-beta peptide oligomers. Neurodegener. Dis. 10, 34-37. doi: 10.1159/000334901
54. Schrag, M., Mueller, C., Zabel, M., Crofton, A., Kirsch, W. M., Ghribi, O., et al. (2013). Oxidative stress in blood in Alzheimer's disease and mild cognitive impairment: a meta-analysis. Neurobiol. Dis. 59, 100-110. doi: 10.1016/j.nbd.2013.07.005.
55. 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.
56. Smith, M. A., Zhu, X., Tabaton, M., Liu, G., Mckeel, D. W. Jr., Cohen, M. L., etal. (2010). Increased iron and free radical generation in preclinical Alzheimer disease and mild cognitive impairment. J. Alzheimers Dis. 19, 363-372. doi: 10.3233/JAD-2010-1239
57. Spat, A., Szanda, G., Csordas, G., and Hajnoczky, G. (2008). High-andlow-calcium-dependent mechanisms of mitochondrial calcium signalling. Cell Calcium 44, 51-63. doi: 10.1016/j.ceca.2007.11.015.
58. Szalai, G., Csordas, G., Hantash, B. M., Thomas, A. P., and Hajnoczky, G. (2000). Calcium signal transmission between ryanodine receptors and mitochondria. J. Biol. Chem. 275, 15305-15313. doi: 10.1074/jbc.275.20.15305.
59. Thannickal, V. J., and Fanburg, B. L. (2000). Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L1005-L1028.
60. Thomas, G. M., and Huganir, R. L. (2004). MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5, 173-183. doi: 10.1038/nrn1346.
61. Uneyama, H., Munakata, M., and Akaike, N. (1993). Caffeine response in pyramidal neurons freshly dissociated from rat hippocampus. Brain Res. 604, 24-31. doi: 10.1016/0006-8993(93)90348-Q
62. Wang, X., Su, B., Lee, H. G., Li, X., Perry, G., Smith, M. A., et al. (2009). Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 29, 9090-9103. doi: 10.1523/JNEUROSCI.1357-09.2009.
63. Yan, M.H., Wang, X., and Zhu, X. (2013). Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic. Biol. Med. 62, 90-101. doi: 10.1016/j.freeradbiomed.2012.11.014.
64. Yoon, Y. S., Yoon, D. S., Lim, I. K., Yoon, S. H., Chung, H. Y., Rojo, M., et al. (2006). Formation of elongated giant mitochondria in DFO-induced cellular senescence: involvement of enhanced fusion process through modulation of Fis1. J. Cell. Physiol. 209,468-480. doi: 10.1002/jcp.20753.
65. Yu, T., Jhun, B. S., and Yoon, Y. (2011). High-glucose stimulation increases reactive oxygen species production through the calcium and mitogen-activated protein kinase-mediated activation of mitochondrial fission. Antioxid. Redox Signal. 14, 425-437. doi: 10.1089/ars.2010.3284.
66. Yuan, H., Gerencser, A. A., Liot, G., Lipton, S. A., Ellisman, M., Perkins, G. A., et al. (2007). Mitochondrial fission is an upstream and required event for baxfoci formation in response to nitric oxide in cortical neurons. Cell Death Differ. 14, 462-471. doi: 10.1038/sj.cdd.4402046.
67. 2+ cross-talk. Proc. Natl. Acad. Sci. U.S.A. 108, 2777-2782. doi: 10.1073/pnas.1100735108.
68. Zecca, L., Youdim, M. B., Riederer, P., Connor, J. R., and Crichton, R. R. (2004). Iron, brainageingandneurodegenerative disorders. Nat. Rev. Neurosci. 5,863-873. doi: 10.1038/nrn1537