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Original Articles

L- and T-type calcium channel blockers protect against the inhibitory effects of mipafox on neurite outgrowth and plasticity-related proteins in SH-SY5Y cells

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References

  • Abou-Donia, M. B. 1993. The cytoskeleton as a target for organophosphorus ester-induced delayed neurotoxicity (OPIDN). Chem. Biol. Interact. 87:383–393.
  • Abou-Donia, M. B. 1995. Involvement of cytoskeletal proteins in the mechanisms of organophosphorus ester-induced delayed neurotoxicity. Clin. Exp. Pharmacol. Physiol. 22:358–359.
  • Abou-Donia, M. B., D. M. Lapudla, and E. Suwita. 1988. Cytoskeletal proteins as targets for organophosphorus compound and aliphatic hexacarbon-induced neurotoxicity. Toxicology 49:469–477.
  • Arias, R. L., M. L. Sung, D. Vasylyev, M. Y. Zhang, K. Albinson, K. Kubek, N. Kagan, C. Beyer, Q. Lin, J. M. Dwyer, M. M. Zaleska, M. R. Bowlby, J. Dunlop, and M. Monaghan. 2008. Amiloride is neuroprotective in an MPTP model of Parkinson’s disease. Neurobiol. Dis. 31:334–341.
  • Ballard, R., R. G. Bardsley, and P. J. Buttery. 1988. Changes in the activity of skeletal muscle calcium-activated neutral proteinase (EC 3.4.22.17) and its specific inhibitor in chickens grown at different rates in response to graded levels of dietary protein. Br. J. Nutr. 59:141–147.
  • Batista, B. L., J. L. Rodrigues, J. A. Nunes, V. C. Souza, and F. Barbosa, Jr. 2009. Exploiting dynamic reaction cell inductively coupled plasma mass spectrometry (DRC-ICP-MS) for sequential determination of trace elements in blood using a dilute-and-shoot procedure. Anal. Chim. Acta 639:13–18.
  • Benowitz, L. I., and A. Routtenberg. 1997. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:84–91.
  • Berridge, M. J., P. Lipp, and M. D. Bootman. 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11–21.
  • Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.
  • Browning, M. D., E. M. Dudek, J. L. Rapier, S. Leonard, and R. Freedman. 1993. Significant reductions in synapsin but not synaptophysin specific activity in the brains of some schizophrenics. Biol. Psychiatry 34:529–535.
  • Burnette, W. N. 1981. “Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate–polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112:195–203.
  • Buroker-Kilgore, M., and K. K. Wang. 1993. A Coomassie brilliant blue G-250-based colorimetric assay for measuring activity of calpain and other proteases. Anal. Biochem. 208:387–392.
  • Callen, L., E. Moreno, P. Barroso-Chinea, D. Moreno-Delgado, A. Cortes, J. Mallol, V. Casado, J. L. Lanciego, R. Franco, C. Lluis, E. I. Canela, and P. J. Mccormick. 2012. Cannabinoid receptors CB1 and CB2 form functional heteromers in brain. J. Biol. Chem. 287:20851–22065.
  • Carlson, K., and M. Ehrich. 2001. Organophosphorus compounds alter intracellular F-actin content in SH-SY5Y human neuroblastoma cells. Neurotoxicology 22:819–827.
  • Ceccaldi, P. E., F. Grohovaz, F. Benfenati, E. Chieregatti, P. Greengard, and F. Valtorta. 1995. Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy. J. Cell Biol. 128:905–912.
  • Chen, T., Y. F. Yang, P. Luo, W. Liu, S. H. Dai, X. R. Zheng, Z. Fei, and X. F. Jiang. 2013. Homer1 knockdown protects dopamine neurons through regulating calcium homeostasis in an in vitro model of Parkinson’s disease. Cell Signal 25:2863–2870.
  • Chen, T. S., E. Koutsilieri, and W. D. Rausch. 1995. MPP+ selectively affects calcium homeostasis in mesencephalic cell cultures from embryonal C57/Bl6 mice. J. Neural Transm. Gen. Sect. 100:153–163.
  • Cheung, Y. T., W. K. Lau, M. S. Yu, C. S. Lai, S. C. Yeung, K. F. So, and R. C. Chang. 2009. Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as in vitro model in neurotoxicity research. Neurotoxicology 30:127–135.
  • Chin, L. S., L. Li, A. Ferreira, K. S. Kosik, and P. Greengard. 1995. Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proc. Natl. Acad. Sci. USA. 92:9230–9234.
  • Cho, T., and E. Tiffany-Castiglioni. 2004. Neurofilament 200 as an indicator of differences between mipafox and paraoxon sensitivity in Sy5Y neuroblastoma cells. J. Toxicol. Environ. Health Part A 67:987–1000.
  • Choudhary, S., and K. D. Gill. 2001. Protective effect of nimodipine on dichlorvos-induced delayed neurotoxicity in rat brain(1). Biochem. Pharmacol. 62:1265–1272.
  • Choudhary, S., S. K. Verma, G. Raheja, P. Kaur, K. Joshi, and K. D. Gill. 2006. The L-type calcium channel blocker nimodipine mitigates cytoskeletal proteins phosphorylation in dichlorvos-induced delayed neurotoxicity in rats. Basic Clin. Pharmacol. Toxicol. 98:447–455.
  • Dani, J. W., D. M. Armstrong, and L. I. Benowitz. 1991. Mapping the development of the rat brain by GAP-43 immunocytochemistry. Neuroscience 40:277–287.
  • Das, K. P., T. M. Freudenrich, and W. R. Mundy. 2004. Assessment of PC12 cell differentiation and neurite growth: a comparison of morphological and neurochemical measures. Neurotoxicol. Teratol. 26:397–406.
  • Dwane, S., E. Durack, and P. A. Kiely. 2013. Optimising parameters for the differentiation of SH-SY5Y cells to study cell adhesion and cell migration. BMC Res. Notes 6:366.
  • Ehrich, M., and L. Correll. 1998. Inhibition of carboxylesterases in SH-SY5Y human and NB41A3 mouse neuroblastoma cells by organophosphorus esters. J. Toxicol. Environ. Health Part A 53:385–399.
  • Ehrich, M., L. Correll, and B. Veronesi. 1997. Acetylcholinesterase and neuropathy target esterase inhibitions in neuroblastoma cells to distinguish organophosphorus compounds causing acute and delayed neurotoxicity. Fundam. Appl. Toxicol. 38:55–63.
  • El-Fawal, H. A., L. Correll, L. Gay, and M. Ehrich. 1990. Protease activity in brain, nerve, and muscle of hens given neuropathy-inducing organophosphates and a calcium channel blocker. Toxicol. Appl. Pharmacol. 103:133–142.
  • El-Fawal, H. A., B. S. Jortner, and M. Ehrich. 1989. Effect of verapamil on organophosphorus-induced delayed neuropathy in hens. Toxicol. Appl. Pharmacol. 97:500–511.
  • Emerick, G. L., G. H. Deoliveira, A. C. Dos Santos, and M. Ehrich. 2012. Mechanisms for consideration for intervention in the development of organophosphorus-induced delayed neuropathy. Chem. Biol. Interact. 199:177–184.
  • Emerick, G. L., L. S. Fernandes, E. S. De Paula, F. Barbosa, Jr., N. A. Dos Santos, and A. C. Dos Santos. 2015. In vitro study of the neuropathic potential of the organophosphorus compounds fenamiphos and profenofos: comparison with mipafox and paraoxon. Toxicol. In Vitro 29:1079–1087.
  • Emerick, G. L., R. G. Peccinini, and G. H. De Oliveira. 2010. Organophosphorus-induced delayed neuropathy: a simple and efficient therapeutic strategy. Toxicol. Lett. 192:238–244.
  • Fernandes, L. S., G. L. Emerick, N. A. Dos Santos, E. S. De Paula, F. Barbosa, Jr., and A. C. Dos Santos. 2015. In vitro study of the neuropathic potential of the organophosphorus compounds trichlorfon and acephate. Toxicol. In Vitro 29:522–528.
  • Fernandes, L. S., G. L. Emerick, R. S. Ferreira, N. A. G. Dos Santos, and A. C. Dos Santos. 2017. High concentration of trichlorfon (1 mM) disrupts axonal cytoskeleton and decreases the expression of plasticity-related proteins in SH-SY5Y cells. Toxicol. In Vitro 39:84–92. doi: 10.1016/j.tiv
  • Fletcher, T. L., P. Cameron, P. De Camilli, and G. Banker. 1991. The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11:1617–1626.
  • Hargreaves, A. J., M. J. Fowler, M. Sachana, J. Flaskos, M. Bountouri, I. C. Coutts, P. Glynn, W. Harris, and W. Graham Mclean. 2006. Inhibition of neurite outgrowth in differentiating mouse N2a neuroblastoma cells by phenyl saligenin phosphate: effects on MAP kinase (ERK 1/2) activation, neurofilament heavy chain phosphorylation and neuropathy target esterase activity. Biochem. Pharmacol. 71:1240–1247.
  • Heutelbeck, A. R., C. Bornemann, M. Lange, A. Seeckts, and M. M. Muller. 2016. Acetylcholinesterase and neuropathy target esterase activities in 11 cases of symptomatic flight crew members after fume events. J. Toxicol. Environ. Health Part A 79:1050–1056.
  • Hirano, Y., H. A. Fozzard, and C. T. January. 1989. Characteristics of L- and T-type Ca2+ currents in canine cardiac Purkinje cells. Am. J. Physiol. 256:1478–1492.
  • Hong, M. S., S. J. Hong, R. Barhoumi, R. C. Burghardt, K. C. Donnelly, J. R. Wild, V. Venkatraj, and E. Tiffany-Castiglioni. 2003. Neurotoxicity induced in differentiated SK-N-SH-SY5Y human neuroblastoma cells by organophosphorus compounds. Toxicol. Appl. Pharmacol. 186:110–118.
  • Husain, K. 2014. Delayed neurotoxicity of organophosphorus compounds. J. Environ. Immunol. Toxicol. 1:1–7.
  • Johnson, M. K. 1974. The primary biochemical lesion leading to the delayed neurotoxic effects of some organophosphorus esters. J. Neurochem. 23:785–789.
  • Kamakura, K., S. Ishiura, H. Sugita, and Y. Toyokura. 1983. Identification of Ca2+-activated neutral protease in the peripheral nerve and its effects on neurofilament degeneration. J. Neurochem. 40:908–913.
  • Kopecky, B. J., R. Liang, and J. Bao. 2014. T-type calcium channel blockers as neuroprotective agents. Pflugers Arch. 466:757–765.
  • Kropp, T. J., and R. J. Richardson. 2003. Relative inhibitory potencies of chlorpyrifos oxon, chlorpyrifos methyl oxon, and mipafox for acetylcholinesterase versus neuropathy target esterase. J. Toxicol. Environ. Health Part A 66:1145–1157.
  • Kupsch, A., M. Gerlach, S. C. Pupeter, J. Sautter, A. Dirr, G. Arnold, W. Opitz, H. Przuntek, P. Riederer, and W. H. Oertel. 1995. Pretreatment with nimodipine prevents MPTP-induced neurotoxicity at the nigral, but not at the striatal level in mice. Neuroreport 6:621–625.
  • L’episcopo, F., C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, F. Impagnatiello, and B. Marchetti. 2011. Switching the microglial harmful phenotype promotes lifelong restoration of subtantia nigra dopaminergic neurons from inflammatory neurodegeneration in aged mice. Rejuvenat Res. 14:411–424.
  • Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
  • Lecht, S., E. Rotfeld, H. Arien-Zakay, R. Tabakman, H. Matzner, R. Yaka, P. I. Lelkes, and P. Lazarovici. 2012. Neuroprotective effects of nimodipine and nifedipine in the NGF-differentiated PC12 cells exposed to oxygen-glucose deprivation or trophic withdrawal. Int. J. Dev. Neurosci. 30:465–469.
  • Li, W., and J. E. Casida. 1998. Organophosphorus neuropathy target esterase inhibitors selectively block outgrowth of neurite-like and cell processes in cultured cells. Toxicol. Lett. 98:139–146.
  • Mahmood, T., and P. C. Yang. 2012. Western blot: technique, theory, and trouble shooting. N. Am. J. Med. Sci. 4:429–434.
  • Makhaeva, G. F., L. V. Sigolaeva, L. V. Zhuravleva, A. V. Eremenko, I. N. Kurochkin, V. V. Malygin, and R. J. Richardson. 2003. Biosensor detection of neuropathy target esterase in whole blood as a biomarker of exposure to neuropathic organophosphorus compounds. J. Toxicol. Environ. Health Part A 66:599–610.
  • Meredith, C., and M. K. Johnson. 1988. Neuropathy target esterase: rates of turnover in vivo following covalent inhibition with phenyl di-n-pentylphosphinate. J. Neurochem. 51:1097–1101.
  • Murgia, M., C. Giorgi, P. Pinton, and R. Rizzuto. 2009. Controlling metabolism and cell death: at the heart of mitochondrial calcium signalling. J. Mol. Cell. Cardiol. 46:781–788.
  • Muzardo, G. A., R. G. Machado, and G. H. De Oliveira. 2008. Effects of calcium gluconate and PMSF in the treatment of acute intoxication of chicken by TOCP. Hum. Exp. Toxicol. 27:247–252.
  • Nielander, H. B., F. Onofri, E. Schaeffer, A. Menegon, R. Fesce, F. Valtorta, P. Greengard, and F. Benfenati. 1997. Phosphorylation-dependent effects of synapsin IIa on actin polymerization and network formation. Eur. J. Neurosci. 9:2712–2722.
  • Obata, T. 2003. Calcium overload enhances hydroxyl radical generation by 1-methyl-4 phenylpyridinium ion (MPP+) in rat striatum. Brain Res. 965:287–289.
  • Piao, F., T. Yamauchi, and N. Ma. 2003. The effect of Calcicol as calcium tonic on delayed neurotoxicity induced by organophosphorus compounds. Toxicol. Lett. 143:65–71.
  • Raghunath, M., R. Patti, P. Bannerman, C. M. Lee, S. Baker, L. N. Sutton, P. C. Phillips, and C. Damodar Reddy. 2000. A novel kinase, AATYK induces and promotes neuronal differentiation in a human neuroblastoma (SH-SY5Y) cell line. Brain Res. Mol. Brain Res. 77:151–162.
  • Rasband, W. S. 1997-2014. Bethesda, Maryland, USA: ImageJ, U. S. National Institutes of Health. http://imagej.nih.gov/ij/.
  • Sachana, M., J. Flaskos, E. Alexaki, P. Glynn, and A. J. Hargreaves. 2001. The toxicity of chlorpyrifos towards differentiating mouse N2a neuroblastoma cells. Toxicol. In Vitro 15:369–372.
  • Schlaepfer, W. W., and M. B. Hasler. 1979. Characterization of the calcium-induced disruption of neurofilaments in rat peripheral nerve. Brain Res. 168:299–309.
  • Shea, T. B., N. I. Perrone-Bizzozero, M. L. Beermann, and L. I. Benowitz. 1991. Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuritogenesis. J. Neurosci. 11:1685–1690.
  • Simms, B. A., and G. W. Zamponi. 2014. Neuronal voltage-gated calcium channels: structure, function, and dysfunction. Neuron 82:24–45.
  • Sousa, S. R., I. Vetter, L. Ragnarsson, and R. J. Lewis. 2013. Expression and pharmacology of endogenous Cav channels in SH-SY5Y human neuroblastoma cells. PLoS One 8:592–593.
  • Tang, C. M., F. Presser, and M. Morad. 1988. Amiloride selectively blocks the low threshold (T) calcium channel. Science 240:213–215.
  • Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350–4354.
  • Tytgat, J., J. Vereecke, and E. Carmeliet. 1990. Mechanism of cardiac T-type Ca channel blockade by amiloride. J. Pharmacol. Exp. Ther. 254:546–551.
  • Wu, Y. J., and X. F. Leng. 1997. Comparison of effects of verapamil and quercetin on delayed polyneuropathy induced by tri-o-cresyl phosphate in hens. Bull. Environ. Contam. Toxicol. 58:611–618.
  • Zhang Run-Ping, L. J.-P. 2014. Amiloride protects PC12 cells from MPP+ induced injury via autophagy-lysosome pathway. J. Jiangsu Univ. 24:352–359.
  • Zhang, W., G. M. Wang, P. J. Wang, Q. Zhang, and S. H. Sha. 2014. Effects of neural stem cells on synaptic proteins and memory in a mouse model of Alzheimer’s disease. J. Neurosci. Res. 92:185–194.
  • Zundorf, G., and G. Reiser. 2011. Calcium dysregulation and homeostasis of neural calcium in the molecular mechanisms of neurodegenerative diseases provide multiple targets for neuroprotection. Antioxid. Redox Signal. 14:1275–1288.

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