Ionomycin-induced calcium influx induces neurite degeneration in mouse neuroblastoma cells: analysis of a time-lapse live cell imaging system

Free Radical Research

Volumn 50, Issue 11, 2016, Pages 1214-1225

  Nakamura, Saki ^a   Nakanishi, Ayumi ^a   Takazawa, Minami ^a   Okihiro, Shunsuke ^a   Urano, Shiro ^a   Fukui, Koji ^a  

^a SHIBAURA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

calcium; Neurite; oxidative stress

Indexed keywords

CALCIUM; FLUORESCENT DYE; IONOMYCIN; LIPID HYDROPEROXIDE; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL BODY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE; LIPID PEROXIDATION; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEURITE; NEUROBLASTOMA CELL; NONHUMAN; TIME LAPSE IMAGING; ANIMAL; CELL DEATH; METABOLISM; MITOCHONDRION; NEUROBLASTOMA; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; CALCIUM; CELL DEATH; IONOMYCIN; MICE; MITOCHONDRIA; NEURITES; NEUROBLASTOMA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84989261699     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715762.2016.1227074     Document Type: Article

References (53)

1. Butterfield DA., The 2013 SFRBM discovery award:selected discoveries from the butterfield laboratory of oxidative stress and its sequela in brain in cognitive disorders exemplified by Alzheimer disease and chemotherapy induced cognitive impairment. Free Radic Biol Med 2014;74:157–174.
2. Seet RC, Lee CY, Lim EC, Tan JJ, Quek AM, Chong WL, et al. Oxidative damage in Parkinson disease:measurement using accurate biomarkers. Free Radic Biol Med 2010;48:560–566.
3. Floyd RA, Hensley K., Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiol Aging 2002;23:795–807
4. Reiter RJ, Oxidative damage in the central nervous system:protection by melatonin. Prog Neurobiol 1998;56:359–384.
5. Watson SN, Nelson MA, Wildering WC., Redox agents modulate neuronal activity and reproduce physiological aspects of neuronal aging. Neurobiol Aging 2012;33:149–161.
6. Sies H., Oxidative stress:oxidants and antioxidants. Exp Physiol 1997;82:291–295.
7. Omoi NO, Arai M, Saito M, Takatsu H, Shibata A, Fukuzawa K, et al. Influence of oxidative stress on fusion of pre-synaptic plasma membranes of the rat brain with phosphatidyl choline liposomes, and protective effect of vitamin E. J Nutr Sci Vitaminol 2006;52:248–255.
8. Urano S, Asai Y, Makabe S, Matsuo M, Izumiyama N, Ohtsubo K, Endo T., Oxidative injury of synapse and alteration of antioxidative defense systems in rats, and its prevention by vitamin E. Eur J Biochem 1997;245:64–70.
9. Cadenas E, Davies KJ., Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000;29:222–230.
10. Gredilla R, Sanz A, Lopez-Torres M, Barja G., Caloric restriction decreases mitochondrial free radical generation at complex 1 and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J 2001;15:1589–1991.
11. Niki E., Lipid peroxidation:physiological levels and dual biological effects. Free Radic Biol Med 2009;47:469–484.
12. Harman D., Aging:a theory based on free radical and radiation chemistry. J Gerontol 1956;11:298–300.
13. An FM, Chen S, Xu Z, Yin L, Wang Y, Liu AR, et al. Glucagon-like peptide-1 regulates mitochondrial biogenesis and tau phosphorylation against advanced glycation end products-induced neuronal insult:studies in vivo and in vitro. Neuroscience 2015;300:75–84.
14. Masoud ST, Vecchio LM, Bergeron Y, Hossain MM, Nguyen LT, Bermejo MK, et al. Increased expression of the dopamine transporter leads to loss of dopamine neurons, oxidative stress and I-DOPA reversible motor deficits. Neurobiol Dis 2015;74:66–75.
15. Gaki GS, Papavassiliou AG. Oxidative stress-induced signaling pathways implicated in the pathogenesis of Parkinson’s disease. Neuromolecular Med 2014;16:217–230.
16. Zhang L, Bahety P, Ee PL., Wnt co-receptor LRP5/6 overexpression confers protection against hydrogen peroxide-induced neurotoxicity and reduces tau phosphorylation in SH-SY5Y cells. Neurochem Int 2015;87:13–21.
17. Wang M, Li YJ, Ding Y, Zhang HN, Sun T, Zhang K, et al. Silibinin prevents autophagic cell death upon oxidative stress in cortical neurons and cerebral ischemia-reperfusion injury. Mol Neurobiol 2015;53:932–943.
18. Jia J, Ma L, Wu M, Zhang L, Zhang X, Zhai Q, et al. Anandamide protects HT22 cells exposed to hydrogen peroxide by inhibiting CB1 receptor-mediated type 2 NADPH oxidase. Oxid Med Cell Longev 2014;2014:893516.
19. Fukui K, Ushiki K, Takatsu H, Koike T, Urano S., Tocotrienols prevent hydrogen peroxide-induced axon and dendrite degeneration in cerebellar granule cells. Free Radic Res 2012;46:184–193.
20. Fukui K, Takatsu H, Koike T, Urano S., Hydrogen peroxide induces neurite degeneration:prevention by tocotrienols. Free Radic Res 2011;45:681–691.
21. Fukui K, Takatsu H, Shinkai T, Suzuki S, Abe K, Urano S., Appearance of amyloid beta-like substances and delayed-type apoptosis in rat hippocampus CA1 region through aging and oxidative stress. J Alzheimers Dis 2005;8:299–309.
22. Hensley K, Harris-White ME., Redox regulation of autophagy in healthy brain and neurodegeneraion. Neurobiol Dis 2015;84:50–59.
23. Kilinc D, Gallo G, Barbee KA., Mechanical membrane injury induces axonal beading through localized activation of calpain. Exp Neurol 2009;219:553–561.
24. Kim JY, Shen S, Dietz K, He Y, Howell O, Reynold R, Casaccia P., HDAC1 nuclear export induced by pathological conditions is essential for the onset of axonal damage. Nat Neurosci 2010;13:180–189.
25. Fukui K, Sekiguchi H, Takatsu H, Koike T, Koike T, Urano S., Tocotrienol prevents AAPH-induced neurite degeneration in neuro2a cells. Redox Rep 2013;18:238–244.
26. Kantamneni S., Cross-talk and regulation between glutamate and GABAB receptors. Front Cell Neurosci 2015;9:135.
27. 2+ release channels to hippocampal synaptic plasticity and spatial memory:potential redox modulation. Antioxid Redox Signal 2014;21:892–914.
28. Chakroborty S, Stutzmann GE. Calcium channelopathies and Alzheimer’s disease:insight into therapeutic success and failures. Eur J Pharmacol 2014;739:83–95.
29. Suzuki M, Nagai Y, Wada K, Koike T., Calcium leak through ryanodine receptor is involved in neuronal death induced by mutant huntingtin. Biochem Biophys Res Commun 2012;429:18–23.
30. Guerrero-Hernández A, Ávila G, Rueda A., Ryanodine receptors as leak channels. Eur J Pharmacol 2014;739:26–38.
31. Kaneai N, Fukui K, Koike T, Urano S., Changes in the levels of CAM kinase II and synapsin I caused by oxidative stress in the rat brain, and its prevention by vitamin E. Adv Biosci Biotechnol 2011;3:1199–1205.
32. Touma E, Kato S, Fukui K, Koike T., Calpain-mediated cleavage of collapsin response mediator protein (CRMP)-2 during neurite degeneration in mice. Eur J Neurosci 2007;12:3361–3381.
33. Ohkawa H, Ohishi N, Yagi K., Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem 1979;95:351–358.
34. Quijada P, Hariharan N, Cubillo JD, Bala KM, Emathinger JM, Wang BJ, et al. Nuclear calcium/calmodulin-dependent protein kinase II signaling enhances cardiac progenitor cell survival and cardiac lineage commitment. J Biol Chem 2015;290:25411–25426.
35. Bhosale G, Sharpe JA, Sundier SY, Duchen MR., Calcium signaling as a mediator of cell energy demand and a trigger to cell death. Ann N Y Acad Sci 2015;1350:107–116.
36. 2+ overload and neuronal death via JAK/CaN signaling. Cell Calcium 2015;58:286–295.
37. Fernandes HB, Baimbridge KG, Church J, Hayden MR, Raymond LA., Mitochondrial sensitivity and altered calcium handling underlie enhanced NMDA-induced apoptosis in YAC128 model of Huntington’s disease. J Neurosci 2007;27:13614–13623.
38. Marshall J, Wong KY, Rupasinghe CN, Tiwari R, Zhao X, Berberoglu ED, et al. Inhibition of N-methyl-D-aspartate-induced retinal neuronal death by polyarginine peptides is linked to the attenuation of stress-induced hyperpolarization of the inner mitochondrial membrane potential. J Biol Chem 2015;290:22030–22048.
39. Cueva Vargas JL, Osswald IK, Unsain N, Aurousseau MR, Barker PA, Bowie D, Di Polo A., Soluble tumor necrosis factor alpha promotes retinal ganglion cell death in glaucoma via calcium-permeable AMPA receptor activation. J Neurosci 2015;35:12088–12102.
40. 2+ influx triggered by DA-9801 potentiates nerve growth factor-induced neurite outgrowth. ACS Chem Neurosci. [Epub ahead of print]. doi:10.1021/acschemneuro.6b00082.
41. Ogawa M, Kurokawa T, Fujiwara K, Polat OK, Badr H, Takahashi N, Mori Y., Functional and structural divergence in human TRPV1 channel subunits by oxidative cysteine modification. J Biol Chem 2016;291:4197–4210.
42. Endo M., Calcium-induced calcium release in skeletal muscle. Physiol Rev 2009;89:1153–1176.
43. Sandler VM, Barbara JG., Calcium-induced calcium release contributes to action potential-evoked calcium transients in hippocampal CA1 pyramidal neurons. J Neurosci 1999;19:4325–4336.
44. Batandler C, Fontaine E, Kériel C, Leverve XM., Determination of mitochondrial reactive oxygen species:methodological aspects. J Cell Mol Med 2002;6:175–187.
45. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, Kunz WS. Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 2004;279:4127–4135.
46. Zielonka J, Kalyanaraman B., Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation:another inconvenient truth. Free Radic Biol Med 2010;48:983–1001.
47. Shioji K, Oyama Y, Okuma K, Nakagawa H., Synthesis and properties of fluorescence probe for detection of peroxides in mitochondria. Bioorg Med Chem Lett 2010;20:3911–3915.
48. Ma M., Role of calpains in the injury-induced dysfunction and degeneration of the mammalian axon. Neurobiol Dis 2013;60:61–79.
49. Villegas R, Martines NW, Lillo J, Pihan P, Hernandez D, Twiss JL, Court FA., Calcium release from intra-axonal endoplastic reticulum leads to axon degeneration through mitochondrial dysfunction. J Neorusci 2014;34:7179–7189.
50. Littlejohns B, Pasdois P, Duggan S, Bond AR, Heesom K, Jackson CL, et al. Hearts from mice fed a non-obesogenic high-fat diet exhibit changes in their oxidative state, calcium and mitochondria in parallel with increased susceptibility to reperfusion injury. PLoS One 2014;9:e100579.
51. 2+ and monoamines:different behaviour of liver and brain mitochondria in undergoing permeability transition. Amino Acids 2012;42:751–759.
52. Overk CR, Rockenstein E, Florio J, Cheng Q, Masliah E., Differential calcium alterations in animal models of neurodegenerative disease:reversal by FK506. Neuroscience 2015;310:549–560.
53. Fukui K, Masuda A, Hosono A, Suwabe R, Yamashita K, Shinkai T, Urano S., Changes in microtubule-related proteins and autophagy in long-term vitamin E-deficient mice. Free Radic Res 2014;48:649–658.