Neuroprotective and antidepressant-like effects of melatonin in a rotenone-induced Parkinson's disease model in rats

Brain Research

Volumn 1593, Issue , 2014, Pages 95-105

  Bassani, Taysa B ^a   Gradowski, Raisa W ^a   Zaminelli, Tiago ^a   Barbiero, Janaína K ^a   Santiago, Ronise M ^a   Boschen, Suelen L ^a   Da Cunha, Claudio ^a   Lima, Marcelo M S ^a   Andreatini, Roberto ^a   Vital, Maria A B F ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

Antidepressant; Melatonin; Neuroprotective; Parkinson's disease; Rotenone

Indexed keywords

RATTUS;

ANTIDEPRESSANT AGENT; DOPAMINE; MELATONIN; NEUROPROTECTIVE AGENT; NORADRENALIN; ROTENONE; SEROTONIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL; CORPUS STRIATUM; DRUG EFFECTS; MALE; METABOLISM; MOTOR ACTIVITY; PARKINSONIAN DISORDERS; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZATION; SUBSTANTIA NIGRA PARS COMPACTA; WISTAR RAT;

ANIMALS; ANTIDEPRESSIVE AGENTS; CORPUS STRIATUM; DOPAMINE; MALE; MELATONIN; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; NOREPINEPHRINE; PARKINSONIAN DISORDERS; PARS COMPACTA; RANDOM ALLOCATION; RATS, WISTAR; ROTENONE; SEROTONIN; TYROSINE 3-MONOOXYGENASE;

EID: 84916595528     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.09.068     Document Type: Article

References (58)

1. Aarsland, D., Pa˚hlhagen, S., Ballard, C.G., Ehrt, U., Svenningsson, P., 2012. Depression in Parkinson disease - epidemiology, mechanisms and management. Nat. Rev. Neurol. 8, 35-47.
2. Acuña-Castroviejo, D., Coto-Montes, A., Gaia Monti, M., Ortiz, G.G., Reiter, R.J., 1997. Melatonin is protective against MPTP-induced striatal and hippocampal lesions. Life Sci. 60, 23-29.
3. Antolín, I., Mayo, J.C., Sainz, R.M., Del Brío, M.A., Herrera, F., Martína, V., Rodríguez, C., 2002. Protective effect of melatonin in a chronic experimental model of Parkinson's disease. Brain Res. 943, 163-173.
4. Betarbet, R., Sherer, T.B., MacKenzie, G., Garcia-Osuna, M., Panov, A.V., Greenamyre, J.T., 2000. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3 (12), 1301-1306.
5. Binfaré, R.W., Mantovani, M., Budni, J., Santos, A.R.S., Rodrigues, A.L.S., 2010. Involvement of dopamine receptors in the antidepressant-like effect of melatonin in the tail suspension test. Eur. J. Pharmacol. 638, 78-83.
6. Bordet, R., Devos, D., Brique, S., Touitou, Y., Guieu, J.D., Libersa, C., Destée, A., 2003. Study of circadian melatonin secretion pattern at different stages of Parkinson's disease. Clin. Neuropharmacol. 26 (2), 65-72.
7. Braak, H., Del Tredici, K., Rüb, U., de Vos, R.A.I., Jansen Steur, E.N. H., Braak, E., 2003. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197-211.
8. Breen, D.P., Vuono, R., Nawarathna, U., Fisher, K., Shneerson, J.M., Reddy, A.B., Barker, R.A., 2014. Sleep and circadian rhythm regulation in early Parkinson disease. JAMA Neurol. 71 (5), 589-595.
9. Büeler, H., 2009. Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Exp. Neurol. 218, 235-246.
10. Capitelli, C., Sereniki, A., Lima, M.M.S., Reksidler, A.B., Tufik, S., Vital, M.A.B.F., 2008. Melatonin attenuates tyrosine hydroxylase loss and hypolocomotion in MPTP-lesioned rats. Eur. J. Pharmacol. 594, 101-108.
11. Chaudhuri, K.R., Healy, D.G., Schapira, A.H.V., 2006. Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol. 5, 235-245.
12. Coulom, H., Birman, S., 2004. Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J. Neurosci. 24, 10993-10998.
13. Datieva, V.K., Rosinskaia, A.V., Levin, O.S., 2013. The use of melatonin in the treatment of chronic fatigue syndrome and circadian rhythm disorders in Parkinson's disease. Zhurnal Nevrol. Psikhiatrii Im. SS Korsakova 113, 77-81.
14. Dauer, W., Przedborski, S., 2003. Parkinson's disease: mechanisms and models. Neuron 39, 889-909.
15. Detanico, B.C., Piato, A.L., Freitas, J.J., Lhullier, F.L., Hidalgo, M.P., Caumo, W., Elisabetsky, E., 2009. Antidepressant-like effects of melatonin in the mouse chronic mild stress model. Eur. J. Pharmacol. 607, 121-125.
16. Hardeland, R., Cardinali, D.P., Srinivasan, V., Spence, D.W., Brown, G.M., Pandi-Perumal, S.R., 2011. Melatonin - a pleiotropic, orchestrating regulator molecule. Prog. Neurobiol. 9, 350-384.
17. Hawkes, C.H., Del Tredici, K., Braak, H., 2010. A timeline for Parkinson's disease. Parkinsonism Relat. Disord. 16, 79-84.
18. Hayashi, A., Matsunaga, N., Okazaki, H., Kakimoto, K., Kimura, Y., Azuma, H., Ikeda, E., Shiba, T., Yamato, M., Yamada, K., Koyanagi, S., Ohdo, S., 2013. A disruption mechanism of the molecular clock in a MPTP mouse model of Parkinson's disease. Neuromol. Med. 15, 238-251.
19. Jin, B., Shin, D.Y., Jeon, M.Y., Gwag, M.R., Baik, H.W., Yoo, K.S., Cho, Y.H., Joo, W.S., Kim, Y.S., Baik, H.H., 1998. Melatonin protects nigral dopaminergic neurons from 1-methyl-4-phenylpyridinium (MPP+) neurotoxicity in rats. Neurosci. Lett. 245, 61-64.
20. Karatsoreos, I.N., 2014. Links between circadian rhythms and psychiatric disease. Front. Behav. Neurosci. 8, 1-5, http://dx.doi.org/10.3389/fnbeh.2014.00162.
21. Lax, P., Esquiva, G., Esteve-Rudd, J., Otalora, B.B., Madrid, J.A., Cuenca, N., 2012. Circadian dysfunction in a rotenone-induced Parkinsonian rodent model. Chronobiol. Int. 29 (2), 147-156.
22. Lin, C.H., Huang, J.Y., Ching, C.H., Chuang, J.I., 2008. Melatonin reduces the neuronal loss, downregulation of dopamine transporter, and upregulation of D2 receptor in rotenoneinduced parkinsonian rats. J. Pineal Res. 44, 205-213.
23. Lin, L., Meng, T., Liu, T.T., Zheng, Z., 2013. Increased melatonin may play dual roles in the striata of a 6-hydroxydopamine model of Parkinson's disease. Life Sci. 92, 311-316.
24. Lin, L., Du, Y., Yuan, S., Shen, J., Lin, X., Zheng, Z., 2014. Serum melatonin is an alternative index of Parkinson's disease severity. Brain Res. 1547, 43-48.
25. Long-Smith, C.M., Sullivan, A.M., Nolan, Y.M., 2009. The influence of microglia on the pathogenesis of Parkinson's disease. Prog. Neurobiol. 89, 277-287.
26. Ma, J., Shaw, V.E., Mitrofanis, J., 2009. Does melatonin help save dopaminergic cells in MPTP-treated mice?. Parkinsonism Relat. Disord. 15, 307-314.
27. Mantovani, M., Pértile, R., Calixto, J.B., Santos, A.R., Rodrigues, A. L.S., 2003. Melatonin exerts an antidepressant-like effect in the tail suspension test in mice: evidence for involvement of N-methyl-D-aspartate receptors and the L-arginine-nitric oxide pathway. Neurosci. Lett. 343, 1-4.
28. Maurizi, C.P., 1990. The therapeutic potential for tryptophan and melatonin: possible roles in depression, sleep, Alzheimer's disease and abnormal aging. Med. Hypotheses 31, 233-242.
29. McMillan, C.R., Sharma, R., Ottenhof, T., Niles, L.P., 2007. Modulation of tyrosine hydroxylase expression by melatonin in human SH-SY5Y neuroblastoma cells. Neurosci. Lett. 419, 202-206.
30. Medeiros, C.A., Cavelhedo de Bruin, P.F., Lopes, L.A., Magalhaes, M.C., de Lourdes Seabra, M., Sales de Bruin, V.M., 2007. Effects of exogenous melatonin on sleep and motor dysfunction in PD: a randomized, double-blind, placebo controlled study. J. Neurol. 254, 459-464.
31. Micale, V., Arezzi, A., Rampello, L., Drago, F., 2006. Melatonin affects the immobility time of rats in the forced swim test: the role of serotonin neurotransmission. Eur. Neuropsychopharmacol. 16, 538-545.
32. Morais, L.H., Lima, M.M.S., Martynhak, B.J., Santiago, R., Takahashi, T.T., Ariza, D., Barbiero, J.K., Andreatini, R., Vital, M.A.B.F., 2012. Characterization of motor, depressive-like and neurochemical alterations induced by a short-term rotenone administration. Pharmacol. Rep. 64, 1081-1090.
33. Moreira, C.G., Barbiero, J.K., Ariza, D., Dombrowski, P.A., Sabioni, P., Bortolanza, M., Da Cunha, C., Vital, M.A.B.F., Lima, M.M.S., 2012. Behavioral, neurochemical and histological alterations promoted by bilateral intranigral rotenone administration: a new approach for an old neurotoxin. Neurotox. Res. 21, 291-301.
34. Pandi-Perumal, S.R., BaHammam, A.S., Brown, G.M., Warren Spence, D., Bharti, V.K., Kaur, C., Hardeland, R., Cardinali, D.P., 2013. Melatonin antioxidative defense: therapeutical implications for aging and neurodegenerative processes. Neurotox. Res. 23, 267-300.
35. Patki, G., Lau, Y., 2011. Melatonin protects against neurobehavioral and mitochondrial deficits in a chronic mouse model of Parkinson's disease. Pharmacol. Biochem. Behav. 99, 704-711.
36. Paus, S., Schmitz-Hübsch, T., Wullner, U., Vogel, A., Klockgether, T., Abele, M., 2007. Bright light therapy in PD: a pilot study. Mov. Disord. 22, 1495-1498.
37. Paxinos, G., Watson, C., 2005. In: The Rat Brain in Stereotaxic Coordinates 5th ed. Academic Press, San Diego.
38. Picillo, M., Rocco, M., Barone, P., 2009. Dopamine receptor agonists and depression in Parkinson's disease. Parkinsonism Relat. Disord. 15S, S81-S84.
39. Porsolt, R.D., Anton, G., Blavet, N., Jalfre, M., 1978. Behavioral despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 47, 379-391.
40. Raghavendra, V., Kaur, G., Kulkarni, S.K., 2000. Anti-depressant action of melatonin in chronic forced swimming-induced behavioral despair in mice, role of peripheral benzodiazepine receptor modulation. Eur. Neuropsychopharmacol. 10, 473-481.
41. Reneric, J.P., Bouvard, M., Stinus, L., 2002. In the rat forced swimming test, chronic but not subacute administration of dual 5-HT/NA antidepressant treatments may produce greater effects than selective drugs. Behav. Brain Res. 136, 521-532.
42. Sanders, L.H., Greenamyre, J.T., 2013. Oxidative damage to macromolecules in human Parkinson disease and the rotenone model. Free Radic. Biol. Med. 62, 111-120.
43. Santiago, R.M., Barbieiro, J., Lima, M.M.S., Dombrowski, P.A., Andreatini, R., Vital, M.A.B.F., 2010. Depressive-like behaviors alterations induced by intranigral MPTP, 6-OHDA, LPS and rotenone models of Parkinson's disease are predominantly associated with serotonin and dopamine. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 1104-1114.
44. Saravanan, K.S., Sindhu, K.M., Mohanakumar, K.P., 2007. Melatonin protects against rotenone-induced oxidative stress in a hemiparkinsonian rat model. J. Pineal Res. 42, 247-253.
45. Shaji, A.V., Kulkarni, S.K., 1998. Central nervous system depressant activities of melatonin in rats and mice. Indian J. Exp. Biol. 36 (3), 257-263.
46. Sharma, R., McMillan, C.R., Tenn, C.C., Niles, L.P., 2006. Physiological neuroprotection by melatonin in a 6- hydroxydopamine model of Parkinson's disease. Brain Res. 1068, 230-236.
47. Sherer, T.B., Kim, J., Betarbet, R., Greenamyre, J.T., 2003. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and innodataalpha-synuclein aggregation. Exp. Neurol. 179, 9-16.
48. Singhal, N.K., Srivastava, G., Agrawal, S., Jain, S.K., Singh, M.P., 2012. Melatonin as a neuroprotective agent in the rodent models of Parkinson's disease: is it all set to irrefutable clinical translation?. Mol. Neurobiol. 45, 186-199.
49. Tapias, V., Cannon, J.R., Greenamyre, J.T., 2010. Melatonin treatment potentiates neurodegeneration in a rat rotenone Parkinson's disease model. J. Neurosci. Res. 88, 420-427.
50. Videnovic, A., Golombek, D., 2013. Circadian and sleep disorders in Parkinson's disease. Exp. Neurol. 243, 45-56.
51. Willis, G.L., Armstrong, S.M., 1999. A therapeutic role for melatonin antagonism in experimental models of Parkinson's disease. Physiol. Behav. 66 (5), 785-795.
52. Willis, G.L., Robertson, A.D., 2004. Recovery of experimental Parkinson's disease with the melatonin analogues ML-23 and S-20928 in a chronic, bilateral 6-OHDA model: a new mechanism involving antagonism of the melatonin receptor. Pharmacol. Biochem. Behav. 79, 413-429.
53. Willis, G.L., Robertson, A.D., 2005. Recovery from experimental Parkinson's disease in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride treated marmoset with the melatonin analogue ML-23. Pharmacol. Biochem. Behav. 80, 9-26.
54. Willis, G.L., 2008. Intraocular microinjections repair experimental Parkinson's disease. Brain Res. 1217, 119-131.
55. Willis, G.L., Moore, C., Armstrong, S.M., 2012. A historical justification for and retrospective analysis of the systematic application of light therapy in Parkinson's disease. Rev. Neurosci. 23 (2), 199-226.
56. Willis, G.L., Moore, C., Armstrong, S.M., 2014. Parkinson's disease, lights and melanocytes: looking beyond the retina. Sci. Rep. Nat. 4, 3291, http://dx.doi.org/10.1038/srep03291.
57. Willison, L.D., Kudo, T., Loh, D.H., Kuljis, D., Colwell, C.S., 2013. Circadian dysfunction may be a key component of the nonmotor symptoms of Parkinson's disease: insights from a transgenic mouse model. Exp. Neurol. 243, 57-66.
58. Zhou, H., Chen, J., Lu, X., Shen, C., Zeng, J., Chen, L., Pei, Z., 2012. Melatonin protects against rotenone-induced cell injury via inhibition of Omi and Bax-mediated autophagy in Hela cells. J. Pineal Res. 52, 120-127.