Passiflora cincinnata Extract Delays the Development of Motor Signs and Prevents Dopaminergic Loss in a Mice Model of Parkinson’s Disease
This article is part of Special Issue:
Luiz Eduardo Mateus Brandão,
Diana Aline Morais Ferreira Nôga,
Aline Lima Dierschnabel,
Clarissa Loureiro das Chagas Campêlo,
Ywlliane da Silva Rodrigues Meurer,
Ramón Hypolito Lima,
Rovena Clara Galvão Januário Engelberth,
Jeferson Souza Cavalcante,
Clésio Andrade Lima,
Murilo Marchioro,
Charles dos Santos Estevam,
José Ronaldo Santos,
Regina Helena Silva,
Alessandra Mussi Ribeiro,
Luiz Eduardo Mateus Brandão
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorDiana Aline Morais Ferreira Nôga
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorAline Lima Dierschnabel
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorClarissa Loureiro das Chagas Campêlo
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorYwlliane da Silva Rodrigues Meurer
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorRamón Hypolito Lima
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorRovena Clara Galvão Januário Engelberth
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorJeferson Souza Cavalcante
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorClésio Andrade Lima
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorMurilo Marchioro
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorCharles dos Santos Estevam
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorJosé Ronaldo Santos
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorRegina Helena Silva
Universidade Federal de São Paulo, São Paulo, SP, Brazil unifesp.br
Search for more papers by this authorCorresponding Author
Alessandra Mussi Ribeiro
Universidade Federal de São Paulo, Santos, SP, Brazil unifesp.br
Search for more papers by this authorLuiz Eduardo Mateus Brandão,
Diana Aline Morais Ferreira Nôga,
Aline Lima Dierschnabel,
Clarissa Loureiro das Chagas Campêlo,
Ywlliane da Silva Rodrigues Meurer,
Ramón Hypolito Lima,
Rovena Clara Galvão Januário Engelberth,
Jeferson Souza Cavalcante,
Clésio Andrade Lima,
Murilo Marchioro,
Charles dos Santos Estevam,
José Ronaldo Santos,
Regina Helena Silva,
Alessandra Mussi Ribeiro,
Luiz Eduardo Mateus Brandão
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorDiana Aline Morais Ferreira Nôga
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorAline Lima Dierschnabel
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorClarissa Loureiro das Chagas Campêlo
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorYwlliane da Silva Rodrigues Meurer
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorRamón Hypolito Lima
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorRovena Clara Galvão Januário Engelberth
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorJeferson Souza Cavalcante
Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil ufrn.br
Search for more papers by this authorClésio Andrade Lima
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorMurilo Marchioro
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorCharles dos Santos Estevam
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorJosé Ronaldo Santos
Universidade Federal de Sergipe, São Cristóvão, SE, Brazil ufs.br
Search for more papers by this authorRegina Helena Silva
Universidade Federal de São Paulo, São Paulo, SP, Brazil unifesp.br
Search for more papers by this authorCorresponding Author
Alessandra Mussi Ribeiro
Universidade Federal de São Paulo, Santos, SP, Brazil unifesp.br
Search for more papers by this authorAcademic Editor: Gunhyuk Park
Abstract
Passiflora cincinnata Masters is a Brazilian native species of passionflower. This genus is known in the American continent folk medicine for its diuretic and analgesic properties. Nevertheless, few studies investigated possible biological effects of P. cincinnata extracts. Further, evidence of antioxidant actions encourages the investigation of possible neuroprotective effects in animal models of neurodegenerative diseases. This study investigates the effect of the P. cincinnata ethanolic extract (PAS) on mice submitted to a progressive model of Parkinson’s disease (PD) induced by reserpine. Male (6-month-old) mice received reserpine (0.1 mg/kg, s.c.), every other day, for 40 days, with or without a concomitant treatment with daily injections of PAS (25 mg/kg, i.p.). Catalepsy, open field, oral movements, and plus-maze discriminative avoidance evaluations were performed across treatment, and immunohistochemistry for tyrosine hydroxylase was conducted at the end. The results showed that PAS treatment delayed the onset of motor impairments and prevented the occurrence of increased catalepsy behavior in the premotor phase. However, PAS administration did not modify reserpine-induced cognitive impairments. Moreover, PAS prevented the decrease in tyrosine hydroxylase immunostaining in the substantia nigra pars compacta (SNpc) induced by reserpine. Taken together, our results suggested that PAS exerted a neuroprotective effect in a progressive model of PD.
References
- 1 Appel K., Rose T., Fiebich B., Kammler T., Hoffmann C., and Weiss G., Modulation of the γ-aminobutyric acid (GABA) system by Passiflora incarnata L., Phytotherapy Research. (2011) 25, no. 6, 838–843, 2-s2.0-79957822286, https://doi.org/10.1002/ptr.3352.
- 2 Dhawan K., Dhawan S., and Sharma A., Passiflora: a review update, Journal of Ethnopharmacology. (2004) 94, no. 1, 1–23, https://doi.org/10.1016/j.jep.2004.02.023, 2-s2.0-3242656424.
- 3 Kinrys G., Coleman E., and Rothstein E., Natural remedies for anxiety disorders: potential use and clinical applications, Depression and Anxiety. (2009) 26, no. 3, 259–265, 2-s2.0-63849284109, https://doi.org/10.1002/da.20460.
- 4 Ulmer T. and MacDougal J. M., Passiflora: passionflowers of the world, 2004, 52, Timber Press, Portland, OR, USA, 430, https://doi.org/10.1007/s10535-008-0032-5.
- 5 Muschner V. C., Zamberlan P. M., Bonatto S. L., and Freitas L. B., Phylogeny, biogeography and divergence times in Passiflora (Passifloraceae), Genetics and Molecular Biology. (2012) 35, no. 4, 1036–1043, 2-s2.0-84872436433, https://doi.org/10.1590/S1415-47572012000600019.
- 6 Montanher A. B., Zucolotto S. M., Schenkel E. P., and Fröde T. S., Evidence of anti-inflammatory effects of Passiflora edulis in an inflammation model, Journal of Ethnopharmacology. (2007) 109, no. 2, 281–288, 2-s2.0-33845638284, https://doi.org/10.1016/j.jep.2006.07.031.
- 7 Li H., Zhou P., Yang Q., Shen Y., Deng J., Li L., and Zhao D., Comparative studies on anxiolytic activities and flavonoid compositions of Passiflora edulis ′edulis′ and Passiflora edulis ′flavicarpa′, Journal of Ethnopharmacology. (2011) 133, no. 3, 1085–1090, 2-s2.0-79551553433, https://doi.org/10.1016/j.jep.2010.11.039.
- 8 Gupta R. K., Kumar D., Chaudhary A. K., Maithani M., and Singh R., Antidiabetic activity of Passiflora incarnata Linn. in streptozotocin- induced diabetes in mice, Journal of Ethnopharmacology. (2012) 139, no. 3, 801–806, 2-s2.0-84856216605, https://doi.org/10.1016/j.jep.2011.12.021.
- 9 Sathish R., Sahu A., and Natarajan K., Antiulcer and antioxidant activity of ethanolic extract of Passiflora foetida L., Indian Journal of Pharmacology. (2011) 43, no. 3, 336–339, https://doi.org/10.4103/0253-7613.81501, 2-s2.0-79958287063.
- 10 Barbosa P. R., Valvassori S. S., BordignonC. L.Jr., Kappel V. D., Martins M. R., Gavioli E. C., Quevedo J., and Reginatto F. H., The aqueous extracts of Passiflora alata and Passiflora edulis reduce anxiety-related behaviors without affecting memory process in rats, Journal of Medicinal Food. (2008) 11, no. 2, 282–288, https://doi.org/10.1089/jmf.2007.722, 2-s2.0-46749143317.
- 11 Grundmann O., Wang J., McGregor G. P., and Butterweck V., Anxiolytic activity of a phytochemically characterized Passiflora incarnata extract is mediated via the GABAergic system, Planta Medica. (2008) 74, no. 15, 1769–1773, https://doi.org/10.1055/s-0028-1088322, 2-s2.0-58049199482.
- 12 Dhawan K., Kumar S., and Sharma A., Anti-anxiety studies on extracts of Passiflora incarnata Linneaus, Journal of Ethnopharmacology. (2001) 78, no. 2-3, 165–170, 2-s2.0-0034772832, https://doi.org/10.1016/S0378-8741(01)00339-7.
- 13 Dhawan K., Kumar S., and Sharma A., Anxiolytic activity of aerial and underground parts of Passiflora incarnata, Fitoterapia. (2001) 72, no. 8, 922–926, 2-s2.0-0035205823, https://doi.org/10.1016/S0367-326X(01)00322-7.
- 14 da Silva Morrone M., de Assis A. M., da Rocha R. F., Gasparotto J., Gazola A. C., Costa G. M., Zucolotto S. M., Castellanos L. H., Ramos F. A., Schenkel E. P., Reginatto F. H., Gelain D. P., and Moreira J. C. F., Passiflora manicata (Juss.) aqueous leaf extract protects against reactive oxygen species and protein glycation in vitro and ex vivo models, Food and Chemical Toxicology. (2013) 60, 45–51, https://doi.org/10.1016/j.fct.2013.07.028, 2-s2.0-84881523567.
- 15 Montefusco-Pereira C. V., De Carvalho M. J., De Araújo Boleti A. P., Teixeira L. S., Matos H. R., and Lima E. S., Antioxidant, anti-inflammatory, and hypoglycemic effects of the leaf extract from passiflora nitida kunth, Applied Biochemistry and Biotechnology. (2013) 170, no. 6, 1367–1378, 2-s2.0-84879890141, https://doi.org/10.1007/s12010-013-0271-6.
- 16 Rudnicki M., de Oliveira M. R., Veiga Pereira T. D., Reginatto F. H., Dal-Pizzol F., and Fonseca Moreira J. C., Antioxidant and antiglycation properties of Passiflora alata and Passiflora edulis extracts, Food Chemistry. (2007) 100, no. 2, 719–724, 2-s2.0-33745231175, https://doi.org/10.1016/j.foodchem.2005.10.043.
- 17 David J. P., Meira M., David J. M., Brandão H. N., Branco A., de Fátima Agra M., Barbosa M. R. V., de Queiroz L. P., and Giulietti A. M., Radical scavenging, antioxidant and cytotoxic activity of Brazilian Caatinga plants, Fitoterapia. (2007) 78, no. 3, 215–218, 2-s2.0-34047256241, https://doi.org/10.1016/j.fitote.2006.11.015.
- 18 Wondracek D. C., Faleiro F. G., Sano S. M., Vieira R. F., and Agostini-Costa T. D. S., Carotenoid composition in Cerrado passifloras, Revista Brasileira de Fruticultura. (2011) 33, no. 4, 1222–1228, 2-s2.0-84857023833, https://doi.org/10.1590/S0100-29452011000400022.
- 19 Kaulmann A. and Bohn T., Carotenoids, inflammation, and oxidative stress-implications of cellular signaling pathways and relation to chronic disease prevention, Nutrition Research. (2014) 34, no. 11, 907–929, https://doi.org/10.1016/j.nutres.2014.07.010, 2-s2.0-84922400509.
- 20 Dickson D. W., Parkinson’s Disease and Parkinsonism: Neuropathology, Cold Spring Harbor Perspectives in Medicine. (2012) 2, no. 8, a009258–a009258, a009258, https://doi.org/10.1101/cshperspect.a009258, 2-s2.0-84872729641.
- 21 Spillantini M. G., Schmidt M. L., Lee V. M., Trojanowski J. Q., Jakes R., and Goedert M., α-synuclein in Lewy bodies, Nature. (1997) 388, no. 6645, 839–840, https://doi.org/10.1038/42166, 2-s2.0-0030882856.
- 22
Lewandowsky M., Paralysis agitans. In: Lewandowsky’s Handbuch der Neurologie, 1912, Springer, Berlin, Germany, 920–933, https://doi.org/10.1007/978-3-662-36377-5.
10.1007/978-3-662-36377-5_30 Google Scholar
- 23 Trétiakoff C., Contribution à l′étude de l′anatomie pathologique du Locus Niger de soemmering avec quelques déductions relatives à la pathogénie des troubles du tonus musculaire et de la maladie de Parkinson, 1919, Méd.-Paris, https://doi.org/10.1522/cla.doh.typ.
- 24 Holdorff B., Rodrigues e Silva A. M., and Dodel R., Centenary of Lewy bodies (1912-2012)., Journal of neural transmission (Vienna, Austria : 1996). (2013) 120, no. 4, 509–516, 2-s2.0-84886293537, https://doi.org/10.1007/s00702-013-0984-2.
- 25 Nelson A. B. and Kreitzer A. C., Reassessing models of basal ganglia function and dysfunction, Annual Review of Neuroscience. (2014) 37, 117–135, 2-s2.0-84904634327, https://doi.org/10.1146/annurev-neuro-071013-013916.
- 26 Thomas B. and Beal MF., Parkinson’s disease, Human Molecular Genetics. (2007) 16, no. (R2), R183–R194.
- 27 Koppula S., Kumar H., More S. V., Lim H.-W., Hong S.-M., and Choi D.-K., Recent updates in redox regulation and free radical scavenging effects by herbal products in experimental models of Parkinson′s disease, Molecules. (2012) 17, no. 10, 11391–11420, https://doi.org/10.3390/molecules171011391, 2-s2.0-84868152531.
- 28 Müller T., Pharmacokinetic considerations for the use of levodopa in the treatment of parkinson disease: Focus on levodopa/carbidopa/entacapone for treatment of levodopa-associated motor complications, Clinical Neuropharmacology. (2013) 36, no. 3, 84–91, 2-s2.0-84878855779, https://doi.org/10.1097/WNF.0b013e31828f3385.
- 29 Pezzoli G. and Zini M., Levodopa in Parkinson′s disease: From the past to the future, Expert Opinion on Pharmacotherapy. (2010) 11, no. 4, 627–635, 2-s2.0-77249168348, https://doi.org/10.1517/14656561003598919.
- 30 Stowe R., Ives N., Clarke C. E., Deane K., van Hilten, Wheatley K., Gray R., Handley K., and Furmston A., Evaluation of the efficacy and safety of adjuvant treatment to levodopa therapy in Parkinson′s disease patients with motor complications, Cochrane Database of Systematic Reviews, 2010, John Wiley & Sons, Ltd, Chichester, UK, CD007166, 2-s2.0-77955501449.
- 31 Voon V., Napier T. C., Frank M. J., Sgambato-Faure V., Grace A. A., Rodriguez-Oroz M., Obeso J., Bezard E., and Fernagut P., Impulse control disorders and levodopa-induced dyskinesias in Parkinson’s disease: an update, The Lancet Neurology. (2017) 16, no. 3, 238–250, https://doi.org/10.1016/S1474-4422(17)30004-2.
- 32 Wang S., Jing H., Yang H., Liu Z., Guo H., Chai L., and Hu L., Tanshinone i selectively suppresses pro-inflammatory genes expression in activated microglia and prevents nigrostriatal dopaminergic neurodegeneration in a mouse model of Parkinson′s disease, Journal of Ethnopharmacology. (2015) 164, 247–255, 2-s2.0-84923914732, https://doi.org/10.1016/j.jep.2015.01.042.
- 33 Olanow C. W., Stern M. B., and Sethi K., The scientific and clinical basis for the treatment of Parkinson disease (2009), Neurology. (2009) 72, no. 21, S1–S136, https://doi.org/10.1212/WNL.0b013e3181a1d44c, 2-s2.0-66949117423.
- 34 Fernandes V. S., Santos J. R., and Leão A. H., Repeated treatment with a low dose of reserpine as a progressive model of Parkinson′s disease, Behavioural Brain Research. (2012) 231, no. 1, 154–163, https://doi.org/10.1016/j.bbr.2012.03.008.
- 35 Campêlo C. L., Santos J. R., Silva A. F., Dierschnabel A. L., Pontes A., Cavalcante J. S., Ribeiro A. M., and Silva R. H., Exposure to an enriched environment facilitates motor recovery and prevents short-term memory impairment and reduction of striatal BDNF in a progressive pharmacological model of parkinsonism in mice, Behavioural Brain Research. (2017) 328, 138–148, https://doi.org/10.1016/j.bbr.2017.04.028.
- 36 Leão A. H. F. F., Sarmento-Silva A. J., Santos J. R., Ribeiro A. M., and Silva R. H., Molecular, Neurochemical, and Behavioral Hallmarks of Reserpine as a Model for Parkinson′s Disease: New Perspectives to a Long-Standing Model, Brain Pathology. (2015) 25, no. 4, 377–390, 2-s2.0-84931564658, https://doi.org/10.1111/bpa.12253.
- 37 Santos J. R., Cunha J. A. S., Dierschnabel A. L., Campêlo C. L. C., Leão A. H. F. F., Silva A. F., Engelberth R. C. G. J., Izídio G. S., Cavalcante J. S., Abílio V. C., Ribeiro A. M., and Silva R. H., Cognitive, motor and tyrosine hydroxylase temporal impairment in a model of parkinsonism induced by reserpine, Behavioural Brain Research. (2013) 253, 68–77, 2-s2.0-84880930813, https://doi.org/10.1016/j.bbr.2013.06.031.
- 38 Silva R. H. and Frussa-Filho R., The plus-maze discriminative avoidance task: A new model to study memory-anxiety interactions. Effects of chlordiazepoxide and caffeine, Journal of Neuroscience Methods. (2000) 102, no. 2, 117–125, 2-s2.0-0034735715, https://doi.org/10.1016/S0165-0270(00)00289-2.
- 39 Paxinos G. and Franklin K., The Mouse Brain in Stereotaxic Coordinates, 2008, Elsevier Academic Press.
- 40 Moo-Puc R. E., Villanueva-Toledo J., Arankowsky-Sandoval G., Alvarez-Cervera F., and Góngora-Alfaro J. L., Treatment with subthreshold doses of caffeine plus trihexyphenidyl fully restores locomotion and exploratory activity in reserpinized rats, Neuroscience Letters. (2004) 367, no. 3, 327–331, https://doi.org/10.1016/j.neulet.2004.06.022, 2-s2.0-4444360391.
- 41 Kaur S. and Starr M. S., Antiparkinsonian action of dextromethorphan in the reserpine-treated mouse, European Journal of Pharmacology. (1995) 280, no. 2, 159–166, 2-s2.0-0029063028, https://doi.org/10.1016/0014-2999(95)00200-5.
- 42 Colpaert F. C., Pharmacological characteristics of tremor, rigidity and hypokinesia induced by reserpine in rat, Neuropharmacology. (1987) 26, no. 9, 1431–1440, https://doi.org/10.1016/0028-3908(87)90110-9, 2-s2.0-0023241854.
- 43 Hastings T. G., Lewis D. A., and Zigmond M. J., Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections, Proceedings of the National Academy of Sciences of the United States of America. (1996) 93, no. 5, 1956–1961, 2-s2.0-0029933450, https://doi.org/10.1073/pnas.93.5.1956.
- 44 Fuentes P., Paris I., Nassif M., Caviedes P., and Segura-Aguilar J., Inhibition of VMAT-2 and DT-diaphorase induce cell death in a substantia nigra-derived cell line - An experimental cell model for dopamine toxicity studies, Chemical Research in Toxicology. (2007) 20, no. 5, 776–783, 2-s2.0-34250702138, https://doi.org/10.1021/tx600325u.
- 45 Bilska A., Dubiel M., Sokołowska-Jezewicz M., Lorenc-Koci E., and Włodek L., Alpha-lipoic acid differently affects the reserpine-induced oxidative stress in the striatum and prefrontal cortex of rat brain, Neuroscience. (2007) 146, no. 4, 1758–1771, https://doi.org/10.1016/j.neuroscience.2007.04.002, 2-s2.0-34249039316.
- 46 Spina M. B. and Cohen G., Dopamine turnover and glutathione oxidation: implications for Parkinson disease, Proceedings of the National Academy of Sciences. (1989) 86, no. 4, 1398–1400, https://doi.org/10.1073/pnas.86.4.1398.
- 47 Gerlach M., Foley P., and Riederer P., The relevance of preclinical studies for the treatment of Parkinson’s disease, Journal of Neurology. (2003) 250, no. S1, i31–i34, https://doi.org/10.1007/s00415-003-1106-y.
- 48 Carlsson A., Lindqvist M., and Magnusson T., 3,4-Dihydroxyphenylalanine and 5-hydroxytryptophan as reserpine antagonists, Nature. (1957) 180, no. 4596, https://doi.org/10.1038/1801200a0, 2-s2.0-0000428532.
- 49 Dutra R. C., Andreazza A. P., Andreatini R., Tufik S., and Vital M. A. B. F., Behavioral effects of MK-801 on reserpine-treated mice, Progress in Neuro-Psychopharmacology and Biological Psychiatry. (2002) 26, no. 3, 487–495, 2-s2.0-0036200505, https://doi.org/10.1016/S0278-5846(01)00295-0.
- 50 Fisher A., Biggs C. S., Eradiri O., and Starr M. S., Dual effects of L-3,4-dihydroxyphenylalanine on aromatic L-amino acid decarboxylase, dopamine release and motor stimulation in the reserpine- treated rat: Evidence that behaviour is dopamine independent, Neuroscience. (1999) 95, no. 1, 97–111, 2-s2.0-0032747455, https://doi.org/10.1016/S0306-4522(99)00406-6.
- 51 Tadaiesky M. T., Andreatini R., and Vital M. A. B. F., Different effects of 7-nitroindazole in reserpine-induced hypolocomotion in two strains of mice, European Journal of Pharmacology. (2006) 535, no. 1-3, 199–207, 2-s2.0-33645412107, https://doi.org/10.1016/j.ejphar.2006.02.004.
- 52 Teixeira A. M., Trevizol F., Colpo G., Garcia S. C., Charão M., Pereira R. P., Fachinetto R., Rocha J. B. T., and Bürger M. E., Influence of chronic exercise on reserpine-induced oxidative stress in rats: Behavioral and antioxidant evaluations, Pharmacology Biochemistry and Behavior. (2008) 88, no. 4, 465–472, 2-s2.0-84984573494, https://doi.org/10.1016/j.pbb.2007.10.004.
- 53 Giovanni A., Sieber BA., Heikkila RE., and Sonsalla PK., Studies on species sensitivity to the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Part 1: Systemic administration, Journal of Pharmacology and Experimental Therapeutics. (1994) 270, 1000–1007.
- 54 He Z., Jiang Y., Xu H., Jiang H., Jia W., Sun P., and Xie J., High frequency stimulation of subthalamic nucleus results in behavioral recovery by increasing striatal dopamine release in 6-hydroxydopamine lesioned rat, Behavioural Brain Research. (2014) 263, 108–114, 2-s2.0-84896727923, https://doi.org/10.1016/j.bbr.2014.01.014.
- 55 Abílio V. C., Araujo C. C. S., Bergamo M., Calvente P. R. V., D′Almeida V., Ribeiro R. D. A., and Frussa-Filho R., Vitamin E attenuates reserpine-induced oral dyskinesia and striatal oxidized glutathione/reduced glutathione ratio (GSSG/GSH) enhancement in rats, Progress in Neuro-Psychopharmacology and Biological Psychiatry. (2003) 27, no. 1, 109–114, https://doi.org/10.1016/s0278-5846(02)00340-8, 2-s2.0-0037304463.
- 56 Faria R. R., Abílio V. C., Grassl C., Chinen C. C., Ribeiro Negrão L. T., Moraes Vilela De Castro J. P., Fukushiro D. F., Dutra Rodrigues M. S., Zanier Gomes P. H., Registro S., De Cassia De Carvalho R., D′Almeida V., Silva R. H., De Alencar Ribeiro R., and Frussa-Filho R., Beneficial effects of vitamin C and vitamin E on reserpine-induced oral dyskinesia in rats: Critical role of striatal catalase activity, Neuropharmacology. (2005) 48, no. 7, 993–1001, 2-s2.0-18044393222, https://doi.org/10.1016/j.neuropharm.2005.01.014.
- 57 Burger M. E., Alves A., Callegari L., Athayde F. R., Nogueira C. W., Zeni G., and Rocha J. B. T., Ebselen attenuates reserpine-induced orofacial dyskinesia and oxidative stress in rat striatum, Progress in Neuro-Psychopharmacology and Biological Psychiatry. (2003) 27, no. 1, 135–140, 2-s2.0-84984576637, https://doi.org/10.1016/S0278-5846(02)00344-5.
- 58 Bastianetto S., Brouillette J., and Quirion R., Neuroprotective effects of natural products: Interaction with intracellular kinases, amyloid peptides and a possible role for transthyretin, Neurochemical Research. (2007) 32, no. 10, 1720–1725, 2-s2.0-34548755196, https://doi.org/10.1007/s11064-007-9333-x.
- 59 Bloom D. A. and Jaiswal A. K., Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression, The Journal of Biological Chemistry. (2003) 278, no. 45, 44675–44682, https://doi.org/10.1074/jbc.m307633200.
- 60 Komachi H., Yanagisawa K., Shirasaki Y., and Miyatake T., Protein kinase C subspecies in hippocampus and striatum of reserpinized rat brain, Brain Research. (1994) 634, no. 1, 127–130, 2-s2.0-0028084743, https://doi.org/10.1016/0006-8993(94)90265-8.
- 61 Neisewander J. L., Lucki I., and McGonigle P., Neurochemical changes associated with the persistence of spontaneous oral dyskinesia in rats following chronic reserpine treatment, Brain Research. (1991) 558, no. 1, 27–35, 2-s2.0-0025808110, https://doi.org/10.1016/0006-8993(91)90710-D.
- 62 Neisewander J. L., Castañeda E., Davis D. A., Elson H. J., and Sussman A. N., Effects of amphetamine and 6-hydroxydopamine lesions on reserpine-induced oral dyskinesia, European Journal of Pharmacology. (1996) 305, no. 1-3, 13–21, 2-s2.0-0343586513, https://doi.org/10.1016/0014-2999(96)00155-0.
- 63 Reckziegel P., Peroza L. R., Schaffer L. F., Ferrari M. C., de Freitas C. M., Bürger M. E., and Fachinetto R., Gallic acid decreases vacuous chewing movements induced by reserpine in rats, Pharmacology Biochemistry and Behavior. (2013) 104, no. 1, 132–137, https://doi.org/10.1016/j.pbb.2013.01.001, 2-s2.0-84873700943.
- 64 Fernandes V. S., Ribeiro A. M., Melo T. G., Godinho M., Barbosa F. F., Medeiros D. S., Munguba H., and Silva R. H., Memory impairment induced by low doses of reserpine in rats: Possible relationship with emotional processing deficits in Parkinson disease, Progress in Neuro-Psychopharmacology and Biological Psychiatry. (2008) 32, no. 6, 1479–1483, 2-s2.0-47749143204, https://doi.org/10.1016/j.pnpbp.2008.05.004.
- 65 Carvalho R. C., Patti C. C., Takatsu-Coleman A. L., Kameda S. R., Souza C. F., Garcez-do-Carmo L., Abílio V. C., Frussa-Filho R., and Silva R. H., Effects of reserpine on the plus-maze discriminative avoidance task: Dissociation between memory and motor impairments, Brain Research. (2006) 1122, no. 1, 179–183, 2-s2.0-33750724696, https://doi.org/10.1016/j.brainres.2006.09.008.
- 66 Alves C. S. D., Andreatini R., Da Cunha C., Tufik S., and Vital M. A. B. F., Phosphatidylserine reverses reserpine-induced amnesia, European Journal of Pharmacology. (2000) 404, no. 1-2, 161–167, 2-s2.0-0034666623, https://doi.org/10.1016/S0014-2999(00)00607-5.
- 67 Silva R. H., Abílio V. C., Torres-Leite D., Bergamo M., Chinen C. C., Claro F. T., Carvalho R. D. C., and Frussa-Filho R., Concomitant development of oral dyskinesia and memory deficits in reserpine-treated male and female mice, Behavioural Brain Research. (2002) 132, no. 2, 171–177, https://doi.org/10.1016/s0166-4328(01)00409-0, 2-s2.0-0037076459.
- 68 Dujardin K., Blairy S., Defebvre L., Duhem S., Noël Y., Hess U., and Destée A., Deficits in decoding emotional facial expressions in Parkinson′s disease, Neuropsychologia. (2004) 42, no. 2, 239–250, 2-s2.0-0345687865, https://doi.org/10.1016/S0028-3932(03)00154-4.
- 69 Souza R. R., França S. L., Bessa M. M., and Takahashi R. N., The usefulness of olfactory fear conditioning for the study of early emotional and cognitive impairment in reserpine model, Behavioural Processes. (2013) 100, 67–73, 2-s2.0-84883346096, https://doi.org/10.1016/j.beproc.2013.08.008.
- 70 Salgado-Pineda P., Delaveau P., Blin O., and Nieoullon A., Dopaminergic contribution to the regulation of emotional perception, Clinical Neuropharmacology. (2005) 28, no. 5, 228–237, 2-s2.0-27644579119, https://doi.org/10.1097/01.wnf.0000185824.57690.f0.
- 71 Huebl J., Spitzer B., Brücke C., Schönecker T., Kupsch A., Alesch F., Schneider G.-H., and Kühn A. A., Oscillatory subthalamic nucleus activity is modulated by dopamine during emotional processing in Parkinson′s disease, Cortex. (2014) 60, 69–81, 2-s2.0-84910059790, https://doi.org/10.1016/j.cortex.2014.02.019.
- 72 Espejo E. F., Structure of the mouse behaviour on the elevated plus-maze test of anxiety, Behavioural Brain Research. (1997) 86, no. 1, 105–112, 2-s2.0-0030950454, https://doi.org/10.1016/S0166-4328(96)02245-0.
- 73 Holmes A., Parmigiani S., Ferrari P. F., Palanza P., and Rodgers R. J., Behavioral profile of wild mice in the elevated plus-maze test for anxiety, Physiology and Behavior. (2000) 71, no. 5, 509–516, 2-s2.0-0034475077, https://doi.org/10.1016/S0031-9384(00)00373-5.
