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Evidence-Based Complementary and Alternative Medicine
Volume 2015 (2015), Article ID 723431, 11 pages
http://dx.doi.org/10.1155/2015/723431
Research Article

Protective Effects of Aqueous Extract of Luehea divaricata against Behavioral and Oxidative Changes Induced by 3-Nitropropionic Acid in Rats

1Universidade Federal do Pampa (UNIPAMPA), Campus Uruguaiana, Uruguaiana, RS, Brazil
2Departamento de Bioquímica e Biologia Molecular, Centro de Ciências Naturais e Exatas (CCNE), Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil

Received 28 April 2015; Revised 14 August 2015; Accepted 15 September 2015

Academic Editor: Claudia Di Giacomo

Copyright © 2015 Aline Alves Courtes et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M.-C. Chiang, Y. Chern, and R.-N. Huang, “PPARgamma rescue of the mitochondrial dysfunction in Huntington's disease,” Neurobiology of Disease, vol. 45, no. 1, pp. 322–328, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. C. A. Ross, E. H. Aylward, E. J. Wild et al., “Huntington disease: natural history, biomarkers and prospects for therapeutics,” Nature Reviews Neurology, vol. 10, no. 4, pp. 204–216, 2014. View at Publisher · View at Google Scholar
  3. J. Chakraborty, D. N. Nthenge-Ngumbau, U. Rajamma, and K. P. Mohanakumar, “Melatonin protects against behavioural dysfunctions and dendritic spine damage in 3-nitropropionic acid-induced rat model of Huntington's disease,” Behavioural Brain Research, vol. 264, pp. 91–104, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Sandhir and A. Mehrotra, “Quercetin supplementation is effective in improving mitochondrial dysfunctions induced by 3-nitropropionic acid: implications in Huntington's disease,” Biochimica et Biophysica Acta: Molecular Basis of Disease, vol. 1832, no. 3, pp. 421–430, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. D. W. Weir, A. Sturrock, and B. R. Leavitt, “Development of biomarkers for Huntington's disease,” The Lancet Neurology, vol. 10, no. 6, pp. 573–590, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. M.-C. Chiang, H.-M. Chen, Y.-H. Lee et al., “Dysregulation of C/EBPα by mutant Huntingtin causes the urea cycle deficiency in Huntington's disease,” Human Molecular Genetics, vol. 16, no. 5, pp. 483–498, 2007. View at Publisher · View at Google Scholar
  7. A. L. Orr, S. Li, C.-E. Wang et al., “N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking,” The Journal of Neuroscience, vol. 28, no. 11, pp. 2783–2792, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. P. H. Reddy and U. P. Shirendeb, “Mutant huntingtin, abnormal mitochondrial dynamics, defective axonal transport of mitochondria, and selective synaptic degeneration in Huntington's disease,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1822, no. 2, pp. 101–110, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. W. Song, J. Chen, A. Petrilli et al., “Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity,” Nature Medicine, vol. 17, no. 3, pp. 377–382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. A. C. Ludolph, F. He, P. S. Spencer, J. Hammerstad, and M. Sabri, “3-nitropropionic acid-exogenous animal neurotoxin and possible human striatal toxin,” Canadian Journal of Neurological Sciences, vol. 18, no. 4, pp. 492–498, 1991. View at Google Scholar · View at Scopus
  11. I. Túnez, I. Tasset, V. P.-D. La Cruz, and A. Santamaría, “3-nitropropionic acid as a tool to study the mechanisms involved in huntington's disease: past, present and future,” Molecules, vol. 15, no. 2, pp. 878–916, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Brouillet, “The 3-NP model of striatal neurodegeneration,” Current Protocols in Neuroscience, vol. 67, pp. 9.48.1–9.48.14, 2014. View at Google Scholar
  13. D. Colle, D. B. Santos, E. L. G. Moreira et al., “Probucol increases striatal glutathione peroxidase activity and protects against 3-nitropropionic acid-induced pro-oxidative damage in rats,” PLoS ONE, vol. 8, no. 6, Article ID e67658, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Johri, A. Chandra, and M. F. Beal, “PGC-1α, mitochondrial dysfunction, and Huntington's disease,” Free Radical Biology and Medicine, vol. 62, pp. 37–46, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. S. R. Mirandola, D. R. Melo, Â. Saito, and R. F. Castilho, “3-nitropropionic acid-induced mitochondrial permeability transition: comparative study of mitochondria from different tissues and brain regions,” Journal of Neuroscience Research, vol. 88, no. 3, pp. 630–639, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Thangarajan, A. Deivasigamani, S. S. Natarajan, P. Krishnan, and S. K. Mohanan, “Neuroprotective activity of L-theanine on 3-nitropropionic acid-induced neurotoxicity in rat striatum,” International Journal of Neuroscience, vol. 124, no. 9, pp. 673–684, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. Y.-J. Wang, P. Thomas, J.-H. Zhong et al., “Consumption of grape seed extract prevents amyloid-β deposition and attenuates inflammation in brain of an alzheimer's disease mouse,” Neurotoxicity Research, vol. 15, no. 1, pp. 3–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. T. M. Tsang, J. N. Haselden, and E. Holmes, “Metabonomic characterization of the 3-nitropropionic acid rat model of huntington's disease,” Neurochemical Research, vol. 34, no. 7, pp. 1261–1271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Damiano, E. Diguet, C. Malgorn et al., “A role of mitochondrial complex II defects in genetic models of Huntington's disease expressing N-terminal fragments of mutant huntingtin,” Human Molecular Genetics, vol. 22, no. 19, pp. 3869–3882, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. B. Khan, M. M. Khan, A. Khan et al., “Naringenin ameliorates Alzheimer's disease (AD)-type neurodegeneration with cognitive impairment (AD-TNDCI) caused by the intracerebroventricular-streptozotocin in rat model,” Neurochemistry International, vol. 61, no. 7, pp. 1081–1093, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Uttara, A. V. Singh, P. Zamboni, and R. T. Mahajan, “Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options,” Current Neuropharmacology, vol. 7, no. 1, pp. 65–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. L. P. Arantes, D. Colle, M. L. Machado et al., “Luehea divaricata Mart. anticholinesterase and antioxidant activity in a Caenorhabditis elegans model system,” Industrial Crops and Products, vol. 62, pp. 265–271, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. G. P. Amaral, N. R. de Carvalho, R. P. Barcelos et al., “Protective action of ethanolic extract of Rosmarinus officinalis L. in gastric ulcer prevention induced by ethanol in rats,” Food and Chemical Toxicology, vol. 55, pp. 48–55, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Babbar, H. S. Oberoi, and S. K. Sandhu, “Therapeutic and nutraceutical potential of bioactive compounds extracted from fruit residues,” Critical Reviews in Food Science and Nutrition, vol. 55, no. 3, pp. 319–337, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. T. A. Loomis, A. M. Font, and N. C. Cortes, Fundamentos de Toxicología, Acribia, 1982.
  26. H. Lorenzi and I. P. D. E. D. Flora, Arvores Brasileiras: Manual de Identificação e Cultivo de Plantas Arbóreas Nativas do Brasil, Instituto Plantarum de Estudos da Flora, 1998.
  27. A. E. Bighetti, M. A. Antônio, A. Possenti, M. A. Foglio, M. G. Siqueira, and J. E. de Carvalho, “Efeitos da administração aguda e subcrônica da Luehea divaricata Martus et Zuccarini,” Lecta-USF, vol. 22, no. 1-2, pp. 53–58, 2004. View at Google Scholar
  28. J. C. A. Tanaka, C. C. da Silva, B. P. D. Filho, C. V. Nakamura, J. E. de Carvalho, and M. A. Foglio, “Constituintes químicos de Luehea divaricata Mart. (Tiliaceae),” Química Nova, vol. 28, no. 5, pp. 834–837, 2005. View at Publisher · View at Google Scholar
  29. V. M. Vargas, R. R. Guidobono, and J. A. Henriques, “Genotoxicity of plant extracts,” Memorias do Instituto Oswaldo Cruz, vol. 86, supplement 2, pp. 67–70, 1991. View at Google Scholar · View at Scopus
  30. L. P. Felício, E. M. Silva, V. Ribeiro et al., “Mutagenic potential and modulatory effects of the medicinal plant Luehea divaricata (Malvaceae) in somatic cells of Drosophila melanogaster: SMART/wing,” Genetics and Molecular Research, vol. 10, no. 1, pp. 16–24, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. B. G. Marinho, L. S. M. Miranda, J. Da S. Costa et al., “The antinociceptive properties of the novel compound (±)-trans-4-hydroxy-6-propyl-1-oxocyclohexan-2-one in acute pain in mice,” Behavioural Pharmacology, vol. 24, no. 1, pp. 10–19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Sofi, C. Macchi, R. Abbate, G. F. Gensini, and A. Casini, “Mediterranean diet and health,” BioFactors, vol. 39, no. 4, pp. 335–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. V. M. B. Filho, E. P. Waczuk, J. P. Kamdem et al., “Phytochemical constituents, antioxidant activity, cytotoxicity and osmotic fragility effects of Caju (Anacardium microcarpum),” Industrial Crops and Products, vol. 55, pp. 280–288, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. M. E. Burger, R. Fachinetto, G. Zeni, and J. B. T. Rocha, “Ebselen attenuates haloperidol-induced orofacial dyskinesia and oxidative stress in rat brain,” Pharmacology Biochemistry and Behavior, vol. 81, no. 3, pp. 608–615, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. A. R. S. Santos, R. O. P. De Campos, O. G. Miguel, V. Cechinel-Filho, R. A. Yunes, and J. B. Calixto, “The involvement of K+ channels and Gi/o protein in the antinociceptive action of the gallic acid ethyl ester,” European Journal of Pharmacology, vol. 379, no. 1, pp. 7–17, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. O. Myhre, J. M. Andersen, H. Aarnes, and F. Fonnum, “Evaluation of the probes 2′,7′-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation,” Biochemical Pharmacology, vol. 65, no. 10, pp. 1575–1582, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Publisher · View at Google Scholar · View at Scopus
  38. P. J. Hissin and R. Hilf, “A fluorometric method for determination of oxidized and reduced glutathione in tissues,” Analytical Biochemistry, vol. 74, no. 1, pp. 214–226, 1976. View at Publisher · View at Google Scholar · View at Scopus
  39. O. H. Lowr, N. J. Rosebrough, A. L. Farr, and R. J. Randall, “Protein measurement with the Folin phenol reagent,” The Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951. View at Google Scholar · View at Scopus
  40. A. Dhir, K. K. Akula, and S. K. Kulkarni, “Tiagabine, a GABA uptake inhibitor, attenuates 3-nitropropionic acid-induced alterations in various behavioral and biochemical parameters in rats,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 32, no. 3, pp. 835–843, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. D. K. Bhateja, D. K. Dhull, A. Gill et al., “Peroxisome proliferator-activated receptor-α activation attenuates 3-nitropropionic acid induced behavioral and biochemical alterations in rats: possible neuroprotective mechanisms,” European Journal of Pharmacology, vol. 674, no. 1, pp. 33–43, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. I. Han, Y. You, J. H. Kordower, S. T. Brady, and G. A. Morfini, “Differential vulnerability of neurons in Huntington's disease: the role of cell type-specific features,” Journal of Neurochemistry, vol. 113, no. 5, pp. 1073–1091, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Kumar, H. Kalonia, and A. Kumar, “Possible GABAergic mechanism in the neuroprotective effect of gabapentin and lamotrigine against 3-nitropropionic acid induced neurotoxicity,” European Journal of Pharmacology, vol. 674, no. 2-3, pp. 265–274, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. E. A. Wilhelm, C. F. Bortolatto, C. R. Jesse, and C. Luchese, “Ebselen protects against behavioral and biochemical toxicities induced by 3-nitropropionic acid in rats: correlations between motor coordination, reactive species levels, and succinate dehydrogenase activity,” Biological Trace Element Research, vol. 162, no. 1–3, pp. 200–210, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Jadiswami, H. M. Megha, S. B. Dhadde et al., “Piroxicam attenuates 3-nitropropionic acid-induced brain oxidative stress and behavioral alteration in mice,” Toxicology Mechanisms and Methods, vol. 24, no. 9, pp. 672–678, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. E. T. Menze, A. Esmat, M. G. Tadros, A. B. Abdel-Naim, and A. E. Khalifa, “Genistein improves 3-NPA-induced memory impairment in ovariectomized rats: impact of its antioxidant, anti-inflammatory and acetylcholinesterase modulatory properties,” PLoS ONE, vol. 10, no. 2, Article ID e0117223, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Kumar and A. Kumar, “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,” Journal of Medicinal Food, vol. 12, no. 3, pp. 591–600, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Rezai-Zadeh, D. Shytle, N. Sun et al., “Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice,” The Journal of Neuroscience, vol. 25, no. 38, pp. 8807–8814, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Kumar and A. Kumar, “Possible role of sertraline against 3-nitropropionic acid induced behavioral, oxidative stress and mitochondrial dysfunctions in rat brain,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 33, no. 1, pp. 100–108, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Bueno-Nava, R. Gonzalez-Pina, A. Alfaro-Rodriguez et al., “Recovery of motor deficit, cerebellar serotonin and lipid peroxidation levels in the cortex of injured rats,” Neurochemical Research, vol. 35, no. 10, pp. 1538–1545, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Sandhir, A. Mehrotra, and S. S. Kamboj, “Lycopene prevents 3-nitropropionic acid-induced mitochondrial oxidative stress and dysfunctions in nervous system,” Neurochemistry International, vol. 57, no. 5, pp. 579–587, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Javed, M. M. Khan, A. Ahmad et al., “Rutin prevents cognitive impairments by ameliorating oxidative stress and neuroinflammation in rat model of sporadic dementia of Alzheimer type,” Neuroscience, vol. 210, pp. 340–352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Nassiri-Asl, T. Naserpour Farivar, E. Abbasi et al., “Effects of rutin on oxidative stress in mice with kainic acid-induced seizure,” Journal of integrative medicine, vol. 11, no. 5, pp. 337–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. R. da Silva Nunes, V. F. S. Kahl, M. da Silva Sarmento et al., “Antigenotoxicity and antioxidant activity of Acerola fruit (Malpighia glabra L.) at two stages of ripeness,” Plant Foods for Human Nutrition, vol. 66, no. 2, pp. 129–135, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Gopinath, D. Prakash, and G. Sudhandiran, “Neuroprotective effect of naringin, a dietary flavonoid against 3-Nitropropionic acid-induced neuronal apoptosis,” Neurochemistry International, vol. 59, no. 7, pp. 1066–1073, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. E. de Almeida Jackix, E. B. Monteiro, H. F. Raposo, E. C. Vanzela, and J. Amaya-Farfán, “Taioba (Xanthosoma sagittifolium) leaves: nutrient composition and physiological effects on healthy rats,” Journal of Food Science, vol. 78, no. 12, pp. H1929–H1934, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. D. K. M. Joseph and Muralidhara, “Neuroprotective efficacy of a combination of fish oil and ferulic acid against 3-nitropropionic acid-induced oxidative stress and neurotoxicity in rats: behavioural and biochemical evidence1,” Applied Physiology, Nutrition and Metabolism, vol. 39, no. 4, pp. 487–496, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Katalinic, G. Rusak, J. Domaćinović Barović et al., “Structural aspects of flavonoids as inhibitors of human butyrylcholinesterase,” European Journal of Medicinal Chemistry, vol. 45, no. 1, pp. 186–192, 2010. View at Publisher · View at Google Scholar
  59. C. Ballard, S. Gauthier, A. Corbett, C. Brayne, D. Aarsland, and E. Jones, “Alzheimer's disease,” The Lancet, vol. 377, no. 9770, pp. 1019–1031, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. A. M. Sabogal-Guáqueta, J. I. Muñoz-Manco, J. R. Ramírez-Pineda, M. Lamprea-Rodriguez, E. Osorio, and G. P. Cardona-Gómez, “The flavonoid quercetin ameliorates Alzheimer's disease pathology and protects cognitive and emotional function in aged triple transgenic Alzheimer's disease model mice,” Neuropharmacology, vol. 93, pp. 134–145, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. C.-M. Liu, G.-H. Zheng, C. Cheng, and J.-M. Sun, “Quercetin protects mouse brain against lead-induced neurotoxicity,” Journal of Agricultural and Food Chemistry, vol. 61, no. 31, pp. 7630–7635, 2013. View at Publisher · View at Google Scholar · View at Scopus