Antidepressant-like effect of pramipexole in an inflammatory model of depression

Behavioural Brain Research

Volumn 320, Issue , 2017, Pages 365-373

  Lieberknecht, Vicente ^a   Cunha, Mauricio Peña ^a   Junqueira, Stella Célio ^a   Coelho, Igor dos Santos ^a   de Souza, Luiz Felipe ^a   dos Santos, Adair Roberto Soares ^a   Rodrigues, Ana Lúcia S ^a   Dutra, Rafael Cypriano ^a   Dafre, Alcir Luiz ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Dopamine receptor; Lipopolysaccharide; Mood disorders; Neuroinflammation; Pramipexole

Indexed keywords

3 NITROTYROSINE; HALOPERIDOL; INTERLEUKIN 1BETA; PRAMIPEXOLE; SULPIRIDE; 3-NITROTYROSINE; BENZOTHIAZOLE DERIVATIVE; DOPAMINE RECEPTOR STIMULATING AGENT; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MALONALDEHYDE; TYROSINE;

ADDUCTION; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DEPRESSION; DRUG EFFICACY; DRUG MECHANISM; FEMALE; FORCED SWIM TEST; HIPPOCAMPUS; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ILLNESS BEHAVIOR; LOCOMOTION; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; SWIMMING; TIME FACTOR;

ANIMALS; BENZOTHIAZOLES; BRAIN; DEPRESSION; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; ILLNESS BEHAVIOR; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LOCOMOTION; MALONDIALDEHYDE; MICE; SWIMMING; TIME FACTORS; TYROSINE;

EID: 85006751427     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.11.007     Document Type: Article

References (69)

1. Ammerman, R.T., Chen, J., Mallow, P.J., Rizzo, J.A., Folger, A.T., et al. Annual direct health care expenditures and employee absenteeism costs in high-risk, low-income mothers with major depression. J. Affect. Disord. 190 (2015), 386–394 http://dx.doi.org/10.1016/j.jad.2015.10.025.
2. Wong, J.J., O'Daly, O., Mehta, M.A., Young, A.H., Stone, J.M., Ketamine modulates subgenual cingulate connectivity with the memory-related neural circuit-a mechanism of relevance to resistant depression?. Peer J., 4, 2016, e1710 http://dx.doi.org/10.7717/peerj.1710.
3. Al-Harbi, K.S., Treatment-resistant depression: therapeutic trends, challenges, and future directions. Patient. Prefer. Adherence 6 (2012), 369–388 http://dx.doi.org/10.2147/PPA.S29716.
4. Duman, R.S., Li, N., A neurotrophic hypothesis of depression: role of synaptogenesis in the actions of NMDA receptor antagonists. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 367 (2012), 2475–2484 http://dx.doi.org/10.1098/rstb.2011.0357.
5. Madeeh Hashmi, A., Awais Aftab, M., Mazhar, N., Umair, M., Butt, Z., The fiery landscape of depression: a review of the inflammatory hypothesis. Pak. J. Med. Sci. 29 (2013), 877–884 http://dx.doi.org/10.12669/pjms.293.3357.
6. Brites, D., Fernandes, A., Neuroinflammation and depression: microglia activation, extracellular microvesicles and microRNA dysregulation. Front. Cell. Neurosci. 9 (2015), 476–496 http://dx.doi.org/10.3389/fncel.2015.00476.
7. Moghadasi, A.N., Pourmand, S., Sharifian, M., Minagar, A., Sahraian, M.A., Behavioral neurology of multiple sclerosis and autoimmune encephalopathies. Neurol. Clin. 34 (2016), 17–31 http://dx.doi.org/10.1016/j.ncl.2015.08.002.
8. Yirmiya, R., Rimmerman, N., Reshef, R., Depression as a microglial disease. Trends Neurosci. 38 (2015), 637–658 http://dx.doi.org/10.1016/j.tins.2015.08.001.
9. Sankowski, R., Mader, S., Valdes-Ferrer, S.I., Systemic inflammation and the brain: novel roles of genetic, molecular, and environmental cues as drivers of neurodegeneration. Front. Cell. Neurosci., 9, 2015, 28 http://dx.doi.org/10.3389/fncel.2015.00028.
10. Dantzer, R., O'Connor, J.C., Freund, G.G., Johnson, R.W., Kelley, K.W., From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9 (2008), 46–56 http://dx.doi.org/10.1038/nrn2297.
11. Andre, C., O'Connor, J.C., Kelley, K.W., Lestage, J., Dantzer, R., et al. Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2 3-dioxygenase in response to peripheral lipopolysaccharide administration. J. Neuroimmunol. 200 (2008), 90–99 http://dx.doi.org/10.1016/j.jneuroim.2008.06.011.
12. Bai, L., Zhang, X., Li, X., Liu, N., Lou, F., et al. Somatostatin prevents lipopolysaccharide-induced neurodegeneration in the rat substantia nigra by inhibiting the activation of microglia. Mol. Med. Rep. 12 (2015), 1002–1008 http://dx.doi.org/10.3892/mmr.2015.3494.
13. Schlichter, L.C., Kaushal, V., Moxon-Emre, I., Sivagnanam, V., Vincent, C., The Ca2+ activated SK3 channel is expressed in microglia in the rat striatum and contributes to microglia-mediated neurotoxicity in vitro. J. Neuroinflammation, 7(4), 2010 http://dx.doi.org/10.1186/1742-2094-7-4.
14. Ayala, A., Munoz, M.F., Arguelles, S., Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell. Longev., 2014, 360438 http://dx.doi.org/10.1155/2014/360438.
15. Ashley, A.K., Hinds, A.I., Hanneman, W.H., Tjalkens, R.B., Legare, M.E., DJ-1 mutation decreases astroglial release of inflammatory mediators. Neurotoxicology 52 (2016), 198–203 http://dx.doi.org/10.1016/j.neuro.2015.12.007.
16. Pintado, C., Revilla, E., Vizuete, M.L., Jimenez, S., Garcia-Cuervo, L., et al. Regional difference in inflammatory response to LPS-injection in the brain: role of microglia cell density. J. Neuroimmunol. 238 (2011), 44–51 http://dx.doi.org/10.1016/j.jneuroim.2011.06.017.
17. Hurst, J.K., Whence nitrotyrosine?. J. Clin. Invest. 109 (2002), 1287–1289 http://dx.doi.org/10.1172/JCI15816.
18. Kvernmo, T., Hartter, S., Burger, E., A review of the receptor-binding and pharmacokinetic properties of dopamine agonists. Clin. Ther. 28 (2006), 1065–1078 http://dx.doi.org/10.1016/j.clinthera.2006.08.004.
19. Trenkwalder, C., Winkelmann, J., Inoue, Y., Paulus, W., Restless legs syndrome-current therapies and management of augmentation. Nat. Rev. Neurol. 11 (2015), 434–445 http://dx.doi.org/10.1038/nrneurol.2015.122.
20. Fawcett, J., Rush, A.J., Vukelich, J., Diaz, S.H., Dunklee, L., et al. Clinical experience with high-dosage pramipexole in patients with treatment-resistant depressive episodes in unipolar and bipolar depression. Am. J. Psychiatry 173 (2016), 107–111 http://dx.doi.org/10.1176/appi.ajp.2015.15060788.
21. Hegde, A., Singh, A., Ravi, M., Narayanaswamy, J.C., Math, S.B., Pramipexole in the treatment of refractory depression in a patient with rapid cycling bipolar disorder. Indian J. Psychol. Med. 37 (2015), 473–474 http://dx.doi.org/10.4103/0253-7176.168614.
22. Seppi, K., Weintraub, D., Coelho, M., Perez-Lloret, S., Fox, S.H., et al. The movement disorder society evidence-based medicine review update: treatments for the non-motor symptoms of parkinson's disease. Mov. Disord. 26:Suppl. 3 (2011), S42–S80 http://dx.doi.org/10.1002/mds.23884.
23. Ostadhadi, S., Imran Khan, M., Norouzi-Javidan, A., Dehpour, A.R., Antidepressant effect of pramipexole in mice forced swimming test: a cross talk between dopamine receptor and NMDA/nitric oxide/cGMP pathway. Biomed. Pharmacother. 81 (2016), 295–304 http://dx.doi.org/10.1016/j.biopha.2016.04.026.
24. Berghauzen-Maciejewska, K., Kuter, K., Kolasiewicz, W., Glowacka, U., Dziubina, A., et al. Pramipexole but not imipramine or fluoxetine reverses the depressive-like behaviour in a rat model of preclinical stages of Parkinson's disease. Behav. Brain Res. 271 (2014), 343–353 http://dx.doi.org/10.1016/j.bbr.2014.06.029.
25. Magnard, R., Vachez, Y., Carcenac, C., Krack, P., David, O., et al. What can rodent models tell us about apathy and associated neuropsychiatric symptoms in Parkinson's disease?. Transl. Psychiatry, 6, 2016, e753 http://dx.doi.org/10.1038/tp.2016.17.
26. Serafine, K.M., Briscione, M.A., Riley, A.L., The effects of haloperidol on cocaine-induced conditioned taste aversions. Physiol. Behav. 105 (2012), 1161–1167 http://dx.doi.org/10.1016/j.physbeh.2011.12.014.
27. Cito, M.C., Silva, M.I., Santos, L.K., Fernandes, M.L., Melo, F.H., et al. Antidepressant-like effect of Hoodia gordonii in a forced swimming test in mice: evidence for involvement of the monoaminergic system. Braz. J. Med. Biol. Res. 48 (2015), 57–64 http://dx.doi.org/10.1590/1414-431X20144215.
28. Martin-de-Saavedra, M.D., Budni, J., Cunha, M.P., Gomez-Rangel, V., Lorrio, S., et al. Nrf2 participates in depressive disorders through an anti-inflammatory mechanism. Psychoneuroendocrinology 38 (2013), 2010–2022 http://dx.doi.org/10.1016/j.psyneuen.2013.03.020.
29. Farzi, A., Reichmann, F., Meinitzer, A., Mayerhofer, R., Jain, P., et al. Synergistic effects of NOD1 or NOD2 and TLR4 activation on mouse sickness behavior in relation to immune and brain activity markers. Brain Behav. Immun. 44 (2015), 106–120 http://dx.doi.org/10.1016/j.bbi.2014.08.011.
30. Araki, R., Nishida, S., Hiraki, Y., Li, F., Matsumoto, K., et al. Kamikihito ameliorates lipopolysaccharide-induced sickness behavior via attenuating neural activation, but not inflammation, in the hypothalamic paraventricular nucleus and central nucleus of the amygdala in mice. Biol. Pharm. Bull. 39 (2016), 289–294 http://dx.doi.org/10.1248/bpb.b15-00707.
31. Dunn, A.J., Swiergiel, A.H., Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol. Biochem. Behav. 81 (2005), 688–693 http://dx.doi.org/10.1016/j.pbb.2005.04.019.
32. Xie, Y., Wang, Y., Zhang, T., Ren, G., Yang, Z., Effects of nanoparticle zinc oxide on spatial cognition and synaptic plasticity in mice with depressive-like behaviors. J. Biomed. Sci., 19, 2012, 14 http://dx.doi.org/10.1186/1423-0127-19-14.
33. Fairchild, K.D., Saucerman, J.J., Raynor, L.L., Sivak, J.A., Xiao, Y., et al. Endotoxin depresses heart rate variability in mice: cytokine and steroid effects. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297 (2009), R1019–R1027 http://dx.doi.org/10.1152/ajpregu.00132.2009.
34. Inden, M., Kitamura, Y., Tamaki, A., Yanagida, T., Shibaike, T., et al. Neuroprotective effect of the antiparkinsonian drug pramipexole against nigrostriatal dopaminergic degeneration in rotenone-treated mice. Neurochem. Int. 55 (2009), 760–767 http://dx.doi.org/10.1016/j.neuint.2009.07.009.
35. Joyce, J.N., Woolsey, C., Ryoo, H., Borwege, S., Hagner, D., Low dose pramipexole is neuroprotective in the MPTP mouse model of Parkinson's disease, and downregulates the dopamine transporter via the D3 receptor. BMC Biol. 2 (2004), 22–34 http://dx.doi.org/10.1186/1741-7007-2-22.
36. Lieberknecht, V., Junqueira, S.C., Cunha, M.P., Barbosa de Souza, T.A.L.F., et al. Pramipexole a dopamine D2/D3 receptor-preferring agonist prevents experimental autoimmune encephalomyelitis development in mice. Mol. Neurobiol., 2016, 1–13 http://dx.doi.org/10.1007/s12035-016-9717-5.
37. Schulte-Herbruggen, O., Vogt, M.A., Hortnagl, H., Gass, P., Hellweg, R., Pramipexole is active in depression tests and modulates monoaminergic transmission, but not brain levels of BDNF in mice. Eur. J. Pharmacol. 677 (2012), 77–86 http://dx.doi.org/10.1016/j.ejphar.2011.12.014.
38. Cunha, M.P., Machado, D.G., Capra, J.C., Jacinto, J., Bettio, L.E., et al. Antidepressant-like effect of creatine in mice involves dopaminergic activation. J. Psychopharmacol. 26 (2012), 1489–1501 http://dx.doi.org/10.1177/0269881112447989.
39. Vamvakides, A., [Effect of presynaptic dopaminergic agonism on the immobility of mice in the forced swimming test]. Ann. Pharm. Fr. 57 (1999), 374–379 http://dx.doi.org/APF-09-1999-57-5-0003-4509-101019-ART2.
40. Porsolt, R.D., Bertin, A., Jalfre, M., Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229 (1977), 327–336.
41. Rosa, P.B., Ribeiro, C.M., Bettio, L.E., Colla, A., Lieberknecht, V., et al. Folic acid prevents depressive-like behavior induced by chronic corticosterone treatment in mice. Pharmacol. Biochem. Behav. 127 (2014), 1–6 http://dx.doi.org/10.1016/j.pbb.2014.10.003.
42. Moretti, M., Neis, V.B., Matheus, F.C., Cunha, M.P., Rosa, P.B., et al. Effects of agmatine on depressive-like behavior induced by intracerebroventricular administration of 1-Methyl-4-phenylpyridinium (MPP(+)). Neurotox. Res. 28 (2015), 222–231 http://dx.doi.org/10.1007/s12640-015-9540-1.
43. Gentile, A., Fresegna, D., Federici, M., Musella, A., Rizzo, F.R., et al. Dopaminergic dysfunction is associated with IL-1beta-dependent mood alterations in experimental autoimmune encephalomyelitis. Neurobiol. Dis. 74 (2015), 347–358 http://dx.doi.org/10.1016/j.nbd.2014.11.022.
44. McCutcheon, S.T., Han, D., Troncoso, J., Koliatsos, V.E., Albert, M., et al. Clinicopathological correlates of depression in early Alzheimer's disease in the NACC. Int. J. Geriatr. Psychiatry 31 (2016), 1301–1311 http://dx.doi.org/10.1002/gps.4435.
45. Capuron, L., Dantzer, R., Cytokines and depression: the need for a new paradigm. Brain Behav. Immun. 17:Suppl. 1 (2003), S119–S124 http://dx.doi.org/10.1016/S0889-1591(02)00078-8.
46. DellaGioia, N., Hannestad, J., A critical review of human endotoxin administration as an experimental paradigm of depression. Neurosci. Biobehav. Rev. 34 (2010), 130–143 http://dx.doi.org/10.1016/j.neubiorev.2009.07.014.
47. Slavich, G.M., Irwin, M.R., From stress to inflammation and major depressive disorder: a social signal transduction theory of depression. Psychol. Bull. 140 (2014), 774–815 http://dx.doi.org/10.1037/a0035302.
48. He, H., Geng, T., Chen, P., Wang, M., Hu, J., et al. NK cells promote neutrophil recruitment in the brain during sepsis-induced neuroinflammation. Sci. Rep., 6, 2016, 27711 http://dx.doi.org/10.1038/srep27711).
49. Bruning, C.A., Martini, F., Soares, S.M., Sampaio, T.B., Gai, B.M., et al. m-Trifluoromethyl-diphenyl diselenide, a multi-target selenium compound, prevented mechanical allodynia and depressive-like behavior in a mouse comorbid pain and depression model. Prog. Neuropsychopharmacol. Biol. Psychiatry 63 (2015), 35–46 http://dx.doi.org/10.1016/j.pnpbp.2015.05.011.
50. Skelly, D.T., Hennessy, E., Dansereau, M.A., Cunningham, C., A systematic analysis of the peripheral and CNS effects of systemic LPS, IL-1beta, [corrected] TNF-alpha and IL-6 challenges in C57BL/6 mice. PLoS One, 8, 2013, e69123 http://dx.doi.org/10.1371/journal.pone.0069123.
51. Frenois, F., Moreau, M., O'Connor, J., Lawson, M., Micon, C., et al. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 32 (2007), 516–531 http://dx.doi.org/10.1016/j.psyneuen.2007.03.005.
52. Farbood, Y., Sarkaki, A., Dolatshahi, M., Taqhi Mansouri, S.M., Khodadadi, A., Ellagic acid protects the brain against 6-Hydroxydopamine induced neuroinflammation in a rat model of parkinson's disease. Basic Clin. Neurosci. 6 (2015), 83–89.
53. Imamura, K., Takeshima, T., Nakaso, K., Ito, S., Nakashima, K., Pramipexole has astrocyte-mediated neuroprotective effects against lactacystin toxicity. Neurosci. Lett. 440 (2008), 97–102 http://dx.doi.org/10.1016/j.neulet.2008.05.067.
54. Berghauzen-Maciejewska, K., Wardas, J., Kosmowska, B., Glowacka, U., Kuter, K., et al. Alterations of BDNF and trkB mRNA expression in the 6-hydroxydopamine-induced model of preclinical stages of Parkinson's disease: an influence of chronic pramipexole in rats. PLoS One, 10, 2015, e0117698 http://dx.doi.org/10.1371/journal.pone.0117698.
55. Guilloux, J.P., Douillard-Guilloux, G., Kota, R., Wang, X., Gardier, A.M., et al. Molecular evidence for BDNF- and GABA-related dysfunctions in the amygdala of female subjects with major depression. Mol. Psychiatry 17 (2012), 1130–1142 http://dx.doi.org/10.1038/mp.2011.113.
56. Gawali, N.B., Bulani, V.D., Chowdhury, A.A., Deshpande, P.S., Nagmoti, D.M., et al. Agmatine ameliorates lipopolysaccharide induced depressive-like behaviour in mice by targeting the underlying inflammatory and oxido-nitrosative mediators. Pharmacol. Biochem. Behav. 149 (2016), 1–8 http://dx.doi.org/10.1016/j.pbb.2016.07.004.
57. Pollak, Y., Yirmiya, R., Cytokine-induced changes in mood and behaviour: implications for ‘depression due to a general medical condition', immunotherapy and antidepressive treatment. Int. J. Neuropsychopharmacol. 5 (2002), 389–399 http://dx.doi.org/10.1017/S1461145702003152.
58. Maes, M., Song, C., Yirmiya, R., Targeting IL-1 in depression. Expert Opin. Ther. Targets 16 (2012), 1097–1112 http://dx.doi.org/10.1517/14728222.2012.718331.
59. Hasegawa-Ishii, S., Inaba, M., Umegaki, H., Unno, K., Wakabayashi, K., et al. Endotoxemia-induced cytokine-mediated responses of hippocampal astrocytes transmitted by cells of the brain-immune interface. Sci. Rep., 6, 2016, 25457 http://dx.doi.org/10.1038/srep25457.
60. Fruhauf, P.K., Ineu, R.P., Tomazi, L., Duarte, T., Mello, C.F., et al. Spermine reverses lipopolysaccharide-induced memory deficit in mice. J. Neuroinflammation 12 (2015), 3–14 http://dx.doi.org/10.1186/s12974-014-0220-5.
61. Koo, J.W., Duman, R.S., IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 751–756 http://dx.doi.org/10.1073/pnas.0708092105.
62. Daginakatte, G.C., Gadzinski, A., Emnett, R.J., Stark, J.L., Gonzales, E.R., et al. Expression profiling identifies a molecular signature of reactive astrocytes stimulated by cyclic AMP or proinflammatory cytokines. Exp. Neurol. 210 (2008), 261–267 http://dx.doi.org/10.1016/j.expneurol.2007.10.016.
63. S. Biesmans, T.F. Meert, J.A. Bouwknecht, P.D. Acton, N. Davoodi, et al. Systemic immune activation leads to neuroinflammation and sickness behavior in mice, Mediators Inflamm., 2013, 271359. http://dx.doi.org/10.1155/2013/271359.
64. O'Callaghan, J.P., Kelly, K.A., VanGilder, R.L., Sofroniew, M.V., Miller, D.B., Early activation of STAT3 regulates reactive astrogliosis induced by diverse forms of neurotoxicity. PLoS One, 9, 2014, e102003 http://dx.doi.org/10.1371/journal.pone.0102003.
65. Abdel-Salam, O.M., Youness, E.R., Mohammed, N.A., Morsy, S.M., Omara, E.A., et al. Citric acid effects on brain and liver oxidative stress in lipopolysaccharide-treated mice. J. Med. Food 17 (2014), 588–598 http://dx.doi.org/10.1089/jmf.2013.0065.
66. Li, R., Tong, J., Tan, Y., Zhu, S., Yang, J., et al. Low molecular weight heparin prevents lipopolysaccharide induced-hippocampus-dependent cognitive impairments in mice. Int. J. Clin. Exp. Pathol. 8 (2015), 8881–8891.
67. Ahn, B., Han, B.S., Kim, D.J., Ohshima, H., Immunohistochemical localization of inducible nitric oxide synthase and 3-nitrotyrosine in rat liver tumors induced by N-nitrosodiethylamine. Carcinogenesis 20 (1999), 1337–1344 http://dx.doi.org/10.1093/carcin/20.7.1337.
68. Kaushik, D.K., Thounaojam, M.C., Kumawat, K.L., Gupta, M., Basu, A., Interleukin-1beta orchestrates underlying inflammatory responses in microglia via Kruppel-like factor 4. J. Neurochem. 127 (2013), 233–244 http://dx.doi.org/10.1111/jnc.12382.
69. Miller, A.H., Raison, C.L., The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat. Rev. Immunol. 16 (2016), 22–34 http://dx.doi.org/10.1038/nri.2015.5.