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Research Article

Possible nitric oxide modulation in protective effect of FK-506 against 3-nitropropionic acid-induced behavioral, oxidative, neurochemical, and mitochondrial alterations in rat brain

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Pages 377-392 | Received 25 Oct 2009, Accepted 21 Jan 2010, Published online: 15 Jun 2010

References

  • Alexi, T., Borlongan, C. V., Faull, R. L., Williams, C. E., Clark, R. G., Gluckman, P. D., et al. (2000). Neuroprotective strategies for basal ganglia degeneration: Parkinson’s and Huntington’s diseases. Neurobiology 60:409–413.
  • Andersen, J. K. (2004). Oxidative stress in neurodegeneration: cause or consequence. Nat Med 10:18–25.
  • Arii, T., Kamiya, T., Arii, K., Ueda, M., Nito, C., Katsura, K. I., et al. (2001). Neuroprotective effect of immunosuppressant FK-506 in transient focal ischemia in rat: Therapeutic time window for FK-506 in transient focal ischemia. Neurol Res 23:755–760.
  • Beckman, J. S. (1996). Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9:836–844.
  • Benchoua, A., Trioulier, Y., Diguet, E., Malgorn, C., Gaillard, M.C., Dufour, N., et al. (2008). Dopamine determines the vulnerability of striatal neurons to the N-terminal fragment of mutant Huntington’s through the regulation of mitochondrial complex II. Hum Mol Genet 17:1446–1456.
  • Berman, S. B., Hastings, T. G. (1999). Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson’s disease. J Neurochem 73:1127–1137.
  • Beyer, C. E., Boikess, S., Luo, B., Dawson, L. A. (2002). Comparison of the effects of antidepressants on norepinephrine and serotonin concentrations in the rat frontal cortex: an in-vivo microdialysis study. J Psychopharmacol 16:297–304.
  • Bezprozvanny, I., Hayden, M. R. (2004). Deranged neuronal calcium signaling and Huntington’s disease. Biochem Biophys Res Commun 322:1310–1317.
  • Brouillet, E., Hantraye, P. (1995). Effects of chronic MPTP and 3-nitropropionic acid in nonhuman primates. Curr Opin Neuro 18:469–473.
  • Brown, G. C. (1999). Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1411:351–369.
  • Cowan, C. M., Fan, M. M., Fan, J., Shehadeh, J., Zhang, L. Y., Graham, R. K., et al. (2008). Polyglutamine-modulated striatal calpain activity in YAC transgenic Huntington disease mouse model: impact on NMDA receptor function and toxicity. J Neurosci. 28, 12725–12735.
  • Dawson, T. M., Steiner, J. P., Dawson, V. L., Dinerman, J. L., Uhl, G. R., Snyder, S. H. (1993). Immunosuppressant FK-506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc Natl Acad Sci U S A 90:9808–9812.
  • Deckel, A. W. (2001). Nitric oxide and nitric oxide synthase in Huntington’s disease. J Neurosci Res 64:99–107.
  • Deckel, A. W., Volmer, P., Weiner, R., Gary, K. A., Covault, J., Sasso, D., et al. (2000). Dietary arginine alters time of symptom onset in Huntington’s disease transgenic mice. Brain Res 875:187–195.
  • Deshpande, S. B., Hida, H., Takei, I. N., Masuda, T., Baba, H., Nishino, H. (2006). Involvement of nitric oxide in 3-nitropropionic acid-induced striatal toxicity in rats. Brain Res 1108:205–215.
  • Ghazinezami, B., Rahimpour, S., Gholipour, T., Ghasemi, M., Sadeghipour, H., Mehr, S. E. (2007). Pharmacologic preconditioning of random-pattern skin flap in rats using local cyclosporine and FK-506: interaction with nitric oxide system. Ann Plast Surg 59:435–440.
  • Gornall, A. G., Bardawill, C. J., David, M. M. (1949). Determination of serum proteins by means of the Biuret reaction. J Biol Chem 177:751–756.
  • Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S., Tannebaum, S. R. (1982). Analysis of nitrate, nitrite, and [15N) nitrate in biological fluids. Ann Biochem 126:131–138.
  • Hersch, S. M., Rosas, H. D. (2008). Neuroprotection for Huntington’s disease: ready, set, slow. Neurotherapeutics 5:226–236.
  • Houten, V. B., Woshner, V., Santos, J. H. (2006). Role of mitochondrial DNA in toxic responses to oxidative stress. DNA Rep 5:145–152.
  • Joshi, D., Naidu, P. S., Singh, A., Kulkarni, S. K. (2005). Reversal of triazolam tolerance and withdrawal induced hyperlocomotor activity and anxiety by bupropion in mice. Pharmacology 75:93–97.
  • Kato, S., Nishio, H., Ogura, M., Takeuchi, K. (2007). Tacrolimus (FK-506), an immune suppressive agent, prevents indomethacin-induced small intestinal ulceration in the rat: inhibition of inducible nitric oxide synthase expression. J Pharmacol Sci 103:40–47.
  • King, M. M., Huang, C. Y., Chock, B. P. (1984). Mammalian brain phosphoproteins as substrates for calcineurin. J Biol Chem 259:8080–8083.
  • King, T. E. (1967). Preparation of succinate dehydrogenase and reconstitution of succinate oxidase. Meth Enzymol 10:322–331.
  • King TE, Howard RL (1967) Preparations and properties of soluble NADH dehydrogenases from cardiac muscle. Methods Enzymol 10, 275–284.
  • Klettner, A., Herdegen, T. (2003). FK-506 and its analogs—therapeutic potential for neurological disorders. Curr Drug Targ CNS Neurol Disord 2:153–162.
  • Kono, Y. (1978). Generation of superoxide radical during auto-oxidation of hydroxylamine and an assay of superoxide dismutase. Arch Biochem Biophysics 186:189–195.
  • Kumar, P., Kalonia, H., Kumar, A. (2009). Sesamol attenuate 3-nitropropionic acid-induced Huntington-like behavioral, biochemical, and cellular alterations in rats. J Asian Nat Prod Res 11:439–450.
  • Kumar, P., Kumar, A. (2009a). Possible role of sertraline against 3-nitropropionic acid-induced behavioral, oxidative stress, and mitochondrial dysfunctions in rat brain. Prog Neuropsychopharmacol Biol Psychiatr 33:100–108.
  • Kumar, P., Kumar, A. (2009b). Possible neuroprotective effect of Withania somnifera root extract against 3-nitropropionic acid-induced behavioral, biochemical, and mitochondrial dysfunction in an animal model of Huntington’s disease. J Med Food 12:591–600.
  • Kumar, P., Kumar, A. (2009c). Neuroprotective effect of cyclosporine and FK506 against 3-nitropropionic acid-induced cognitive dysfunction and glutathione redox in rat: possible role of nitric oxide. Neurosci Res 63:302–314.
  • Kumar, P., Padi, S. S., Naidu, P. S., Kumar, A. (2006). Effect of resveratrol on 3-nitropropionic acid-induced biochemical and behavioural changes: possible neuroprotective mechanisms. Behav Pharmacol 17(5–6):485–492.
  • Lee, W. T., Chang, C. (2004). Magnetic resonance imaging and spectroscopy in assessing 3-nitropropionic acid-induced brain lesions: an animal model of Huntington’s disease. Prog Neurobiol 72:87–110.
  • Liu, Y., Peterson, D. A., Kimura, H., Schubert, D. (1997). Mechanisms of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolinium bromide (MTT) reduction. J Neurochem 69:581–593.
  • Luck, H. (1971). Catalase. In: Bergmeyer, H. U. (Eds.), Methods of Enzymatic Analysis (pp 885–893 ), New York: Academic Press.
  • Ludolph, A. C., He, F., Spencer, P. S., Hammerstad, J., Sabri, M. (1991). 3-nitropropionic acid-exogenous animal neurotoxin and possible human striatal toxin. Can J Neurol Sci 18:492–498.
  • Manáková, S., Singh, A., Kääriäinen, T., Taari, H., Kulkarni, S. K., Männistö, P. T. (2005). Failure of FK-506 (tacrolimus) to alleviate apomorphine-induced circling in rat Parkinson model in spite of some cytoprotective effects in SH-SY5Y dopaminergic cell. Brain Res 1038:83–91.
  • Massioui, N., Ouary, S., Chéruel, F., Hantraye, P., Brouillet, E. (2001). Perseverative behavior underlying attentional set-shifting deficits in rats chronically treated with the neurotoxin, 3-nitropropionic acid. Exp Neurol 172:172–181.
  • Mogi, M., Togari, A., Tanaka, K., Ogawa, N., Ichinose, H., Nagatsu, T. (2000). Increase in level of tumor necrosis factor-alpha in 6-hydroxydopamine-lesioned striatum in rats is suppressed by immunosuppressant FK-506. Neurosci Lett 289:165–178.
  • Pandey, M., Varghese, M., Sindhu, K. M., Sreetama, S., Navneet,A. K., Mohanakumar, K. P., et al. (2008). Mitochondrial NAD+-linked state 3 respiration and complex-I activity are compromised in the cerebral cortex of 3-nitropropionic acid-induced rat model of Huntington’s disease. J Neurochem 104:420–434.
  • Pardo, R. L., Colin, E., Régulier E. T., Aebischer P., Déglon N., Humbert S. (2006). Inhibition of calcineurin by FK-506 protects against polyglutamine-Huntington’s toxicity through an increase of Huntington’s phosphorylation at S421. J Neuro 26:1635–1645.
  • Pérez-Severiano, F., Escalante, B., Vergara, P., Ríos, C., Segovia, J. (2002). Age-dependent changes in nitric oxide synthase activity and protein expression in striata of mice transgenic for the Huntington’s disease mutation. Brain Res 951:36–42.
  • Picconi, B., Passino, E., Sgobio, C., Bonsi, P., Barone, I., Ghiglieri, V., et al. (2006). Plastic and behavioral abnormalities in experimental Huntington’s disease: a crucial role for cholinergic interneurons. Neurobiol Dis 22:143–152.
  • Pong, K., Zaleska, M. M. (2003). Therapeutic implications for immunophilin ligands in the treatment of neurodegenerative diseases. Curr Drug Targ CNS Neurol Disord 2:349–356.
  • Pubill, D., Verdaguer, E., Canudas, A. M., Sureda, F. X., Escubedo, E., Camarasa, J., et al. (2001). Orphenadrine prevents 3-nitropropionic acid-induced neurotoxicity in vitro and in vivo. Br J Pharmacol 132:693–702.
  • Reeves, T. M., Phillips, L. L., Lee, N. N., Povlishock, J. T. (2007). Preferential neuroprotective effect of tacrolimus (FK-506) on unmyelinated axons following traumatic brain injury. Brain Res 1154:225–236.
  • Rodríguez-Martínez, E., Rugerio-Vargas, C., Rodríguez, A. I., Borgonio-Pérez, G., Rivas-Arancibia, S. (2004). Antioxidant effects of taurine, vitamin C, and vitamin E on oxidative damage in hippocampus caused by the administration of 3-nitropropionic acid in rats. Int J Neurosci 114:1133–1145.
  • Sabatini, D. M., Lai, M. M., Snyder, S. H. (1997). Neural roles of immunophilins and their ligands. Mol Neurobiol 15:223–239.
  • Sasaki, T., Hamada, J., Shibata, M., Gotoh, J., Araki, N., Fukuuchi, Y. (2004). FK-506 abrogates delayed neuronal death via suppression of nitric oxide production in rats. Brain Res 1009:34–49.
  • Saydoff, J. A., Liu, L. S., Garcia, R. A., Hu, Z., Li, D., von Borstel R.W. (2003). Oral uridine pro-drug PN401 decreases neurodegeneration, behavioral impairment, weight loss, and mortality in the 3-nitropropionic acid mitochondrial toxin model of Huntington’s disease. Brain Res 994:44–54.
  • Sharkey, J., Butcher, S. P., Kelly, J. S. (1994). Endothelin-1 induced middle cerebral artery occlusion: pathological consequences and neuroprotective effects of MK801. J Auton Trans 49:177–185.
  • Sharkey, J., Crawford, J. H., Butcher, S. P., Marston, H. M. (1996). Tacrolimus (FK-506) ameliorates skilled motor deficits produced by middle cerebral artery occlusion in rats. Stroke 27:2282–2296.
  • Singh, A., Naidu, P. S., Kulkarni, S. K. (2003). Possible antioxidant and neuroprotective mechanisms of FK-506 in attenuating haloperidol-induced orofacial dyskinesia. Eur J Pharmacol 477:87–94.
  • Sottocasa, G. L., Kuylenstierna, B., Ernster, L., Bergstrand, A. (1967). An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J Cell Biol 32:415–428.
  • Steiner, J. P., Hamilton, G. S., Ross, D. T., Valentine, H. L., Guo, H., Connolly, M. A. (1997). Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc Natl Acad Sci U S A 94:2019–2024.
  • Takamatsu, H., Tsukada, H., Noda, A., Kakiuchi, T., Nishiyama, S., Nishimura, S., et al. (2001). FK- 506 attenuates early ischemic neuronal death in a monkey model of stroke. J Nucl Med 42:1833–1440.
  • Teunissen, C. E., Markerink-van Ittersum M., de Bruijn C., Steinbusch H. W., de Vente, J. (2002). Evaluation of 3-nitrotyrosine as a marker for 3-nitropropionic acid-induced oxidative stress in Lewis and Wistar rats and strain-specific whole brain spheroid cultures. Brain Res 931:5–20.
  • Toung, T. J., Bhardwaj, A., Dawson, V. L., Dawson, T. M., Traystman, R. J., Hurn, P. D. (1999). Neuroprotective FK-506 does not alter in vivo nitric oxide production during ischemia and early reperfusion in rats. Stroke 30:1279–1285.
  • Túnez, I., Feijóo, M., Collado, J. A., Medina, F. J., Peña, J., Muñoz Mdel, C. et, al. (2007). Effect of testosterone on oxidative stress and cell damage induced by 3-nitropropionic acid in striatum of ovariectomized rats. Life Sci 80:1221–1227.
  • Tunez, I., Montilla, P., Munoz, M. D. C., Feijoo, M., Salcedo, M. (2004). Protective effect of nicotine on 3-nitropropionic acid-induced oxidative stress in synaptosomes in an animal model of Huntington’s disease. Eur J of Pharmacol 504:169–175.
  • Wills, E. D. (1966). Mechanism of lipid peroxide formation in animals. Biochem J 99:667–676.
  • Winter, C., Schenkel, J., Bürger, E., Eickmeier, C., Zimmermann, M., Herdegen, T. (2000). The immunophilin ligand FK-506, but not GPI-1046, protects against neuronal death and inhibits c-Jun expression in the substantia nigra pars compacta following transection of the rat medial forebrain bundle. Neuroscience 95:753–776.
  • Wu, H. Y., Tomizawa, K., Oda, Y., Wei, F. Y., Lu, Y. F., Matsushita, M., et al. (2004). Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J Biol Chem 279:4929–4940.
  • Yao, H., Zhou, J., Li, D., Wu, N., Bader, A., Höxtermann, S. (2005). FK-506 enhances triptolide-induced downregulation of cyclooxygenase-2, inducible nitric oxide synthase, as well as their products PGE2 and NO in TNF-alpha-stimulated synovial fibroblasts from rheumatoid arthritic patients. Eur J Med Res 10:110–116.

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