Pramipexole, a Dopamine D2/D3 Receptor-Preferring Agonist, Prevents Experimental Autoimmune Encephalomyelitis Development in Mice

Molecular Neurobiology

Volumn 54, Issue 2, 2017, Pages 1033-1045

  Lieberknecht, Vicente ^a   Junqueira, Stella C ^a   Cunha, Mauricio P ^a   Barbosa, Thaís A ^a   de Souza, Luiz F ^a   Coelho, Igor S ^a   Santos, Adair R S ^a   Rodrigues, Ana Lúcia S ^a   Dafré, Alcir L ^a   Dutra, Rafael C ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Autoimmunity; Dopamine receptor agonist; Experimental autoimmune encephalomyelitis; Pramipexole

Indexed keywords

ALPHA SYNUCLEIN; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; GLUTATHIONE PEROXIDASE; INTERLEUKIN 17; INTERLEUKIN 1BETA; PARKIN; PRAMIPEXOLE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; BENZOTHIAZOLE DERIVATIVE; DOPAMINE RECEPTOR STIMULATING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CORPUS STRIATUM; CYTOKINE PRODUCTION; DEMYELINATION; DRUG MECHANISM; DRUG RESPONSE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HELPER CELL; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LYMPHOID TISSUE; MACROGLIA; MOTOR DYSFUNCTION; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; SPINAL CORD; AGONISTS; ANIMAL; C57BL MOUSE; IMMUNOLOGY; PATHOLOGY;

ANIMALS; BENZOTHIAZOLES; DOPAMINE AGONISTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; MICE; MICE, INBRED C57BL; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3;

EID: 84955294319     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-016-9717-5     Document Type: Article

References (67)

1. Grigoriadis N, van Pesch V (2015) A basic overview of multiple sclerosis immunopathology. Eur J Neurol 22(Suppl 2):3–13
2. Rosti-Otajarvi E, Hamalainen P (2013) Behavioural symptoms and impairments in multiple sclerosis: a systematic review and meta-analysis. Mult Scler 19:31–45
3. Sawcer S, Franklin RJ, Ban M (2014) Multiple sclerosis genetics. Lancet Neurol 13:700–709
4. Dowling P, Husar W, Menonna J, Donnenfeld H, Cook S, Sidhu M (1997) Cell death and birth in multiple sclerosis brain. J Neurol Sci 149:1–11
5. Zamvil SS, Steinman L (2003) Diverse targets for intervention during inflammatory and neurodegenerative phases of multiple sclerosis. Neuron 38:685–688
6. Pacheco R, Contreras F, Zouali M (2014) The dopaminergic system in autoimmune diseases. Front Immunol 5:117
7. Dijkstra CD, van der Voort ER, De Groot CJ, Huitinga I, Uitdehaag BM, Polman CH, Berkenbosch F (1994) Therapeutic effect of the D2-dopamine agonist bromocriptine on acute and relapsing experimental allergic encephalomyelitis. Psychoneuroendocrinology 19:135–142
8. Khan OA, Olek MJ (1995) Treatment of paroxysmal symptoms in multiple sclerosis with bromocriptine. J Neurol Neurosurg Psychiatry 58:253
9. Riederer P, Wuketich S (1976) Time course of nigrostriatal degeneration in Parkinson’s disease. A detailed study of influential factors in human brain amine analysis. J Neural Transm 38:277–301
10. Nagatsu T, Sawada M (2007) Biochemistry of postmortem brains in Parkinson’s disease: historical overview and future prospects. J Neural Transm Suppl 72:113–120
11. Kustrimovic N, Rasini E, Legnaro M, Marino F, Cosentino M (2014) Expression of dopaminergic receptors on human CD4+ T lymphocytes: flow cytometric analysis of naive and memory subsets and relevance for the neuroimmunology of neurodegenerative disease. J Neuroimmune Pharmacol 9:302–312
12. Papadopoulos D, Ewans L, Pham-Dinh D, Knott J, Reynolds R (2006) Upregulation of alpha-synuclein in neurons and glia in inflammatory demyelinating disease. Mol Cell Neurosci 31:597–612
13. Wang H, Wang K, Xu W, Wang C, Qiu W, Zhong X, Dai Y, Wu A et al (2012) Cerebrospinal fluid alpha-synuclein levels are elevated in multiple sclerosis and neuromyelitis optica patients during replase. J Neurochem 122:19–23
14. Dias V, Junn E, Mouradian MM (2013) The role of oxidative stress in Parkinson’s disease. J Parkinsons Dis 3:461–491
15. Gilgun-Sherki Y, Melamed E, Offen D (2004) The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J Neurol 251:261–268
16. Ferrari-Toninelli G, Maccarinelli G, Uberti D, Buerger E, Memo M (2010) Mitochondria-targeted antioxidant effects of S(-) and R(+) pramipexole. BMC Pharmacol 10:2
17. Inden M, Kitamura Y, Tamaki A, Yanagida T, Shibaike T, Yamamoto A, Takata K, Yasui H et al (2009) Neuroprotective effect of the antiparkinsonian drug pramipexole against nigrostriatal dopaminergic degeneration in rotenone-treated mice. Neurochem Int 55:760–767
18. Stromnes IM, Goverman JM (2006) Active induction of experimental allergic encephalomyelitis. Nat Protoc 1:1810–1819
19. Elhak SG, Ghanem AA, Abdelghaffar H, Eldakroury S, Eltantawy D, Eldosouky S, Salama M (2010) The role of pramipexole in a severe Parkinson’s disease model in mice. Ther Adv Neurol Disord 3:333–337
20. Li C, Guo Y, Xie W, Li X, Janokovic J, Le W (2010) Neuroprotection of pramipexole in UPS impairment induced animal model of Parkinson’s disease. Neurochem Res 35:1546–1556
21. Dutra RC, Bento AF, Leite DF, Manjavachi MN, Marcon R, Bicca MA, Pesquero JB, Calixto JB (2013) The role of kinin B1 and B2 receptors in the persistent pain induced by experimental autoimmune encephalomyelitis (EAE) in mice: evidence for the involvement of astrocytes. Neurobiol Dis 54:82–93
22. Quintao NL, Medeiros R, Santos AR, Campos MM, Calixto JB (2005) The effects of diacerhein on mechanical allodynia in inflammatory and neuropathic models of nociception in mice. Anesth Analg 101:1763–1769
23. Walczak JS, Beaulieu P (2006) Comparison of three models of neuropathic pain in mice using a new method to assess cold allodynia: the double plate technique. Neurosci Lett 399:240–244
24. Freitas AE, Bettio LE, Neis VB, Santos DB, Ribeiro CM, Rosa PB, Farina M, Rodrigues AL (2014) Agmatine abolishes restraint stress-induced depressive-like behavior and hippocampal antioxidant imbalance in mice. Prog Neuropsychopharmacol Biol Psychiatry 50:143–150
25. Hempel SL, Buettner GR, O’Malley YQ, Wessels DA, Flaherty DM (1999) Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 2′,7′-dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-2′,7′-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Radic Biol Med 27:146–159
26. Pacheco R, Prado CE, Barrientos MJ, Bernales S (2009) Role of dopamine in the physiology of T-cells and dendritic cells. J Neuroimmunol 216:8–19
27. Bannerman P, Hahn A, Soulika A, Gallo V, Pleasure D (2007) Astrogliosis in EAE spinal cord: derivation from radial glia, and relationships to oligodendroglia. Glia 55:57–64
28. Williams A, Piaton G, Lubetzki C (2007) Astrocytes—friends or foes in multiple sclerosis? Glia 55:1300–1312
29. Raphael I, Nalawade S, Eagar TN, Forsthuber TG (2015) T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine 74:5–17
30. Steinman RM, Cohn ZA (1973) Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med 137:1142–1162
31. Huang G, Wang Y, Vogel P, Kanneganti TD, Otsu K, Chi H (2012) Signaling via the kinase p38alpha programs dendritic cells to drive TH17 differentiation and autoimmune inflammation. Nat Immunol 13:152–161
32. Lu JQ, Fan Y, Mitha AP, Bell R, Metz L, Moore GR, Yong VW (2009) Association of alpha-synuclein immunoreactivity with inflammatory activity in multiple sclerosis lesions. J Neuropathol Exp Neurol 68:179–189
33. Witte ME, Bol JG, Gerritsen WH, van der Valk P, Drukarch B, van Horssen J, Wilhelmus MM (2009) Parkinson’s disease-associated parkin colocalizes with Alzheimer’s disease and multiple sclerosis brain lesions. Neurobiol Dis 36:445–452
34. Levite M (2015) Dopamine and T cells: receptors, direct and potent effects, endogenous production and abnormalities in autoimmune, neurological and psychiatric diseases. Acta Physiol (Oxf). doi:10.1111/apha.12476
35. Jafari M, Ahangari G, Saberi M, Samangoui S, Torabi R, Zouali M (2013) Distorted expression of dopamine receptor genes in systemic lupus erythematosus. Immunobiology 218:979–983
36. Giorelli M, Livrea P, Trojano M (2005) Dopamine fails to regulate activation of peripheral blood lymphocytes from multiple sclerosis patients: effects of IFN-beta. J Interferon Cytokine Res 25:395–406
37. Kvernmo T, Hartter S, Burger E (2006) A review of the receptor-binding and pharmacokinetic properties of dopamine agonists. Clin Ther 28:1065–1078
38. Barbanti P, Fabbrini G, Ricci A, Cerbo R, Bronzetti E, Caronti B, Calderaro C, Felici L et al (1999) Increased expression of dopamine receptors on lymphocytes in Parkinson’s disease. Mov Disord 14:764–771
39. Donnan GA, Woodhouse DG, Kaczmarczyk SJ, Holder JE, Paxinos G, Chilco PJ, Churchyard AJ, Kalnins RM et al (1991) Evidence for plasticity of the dopaminergic system in parkinsonism. Mol Neurobiol 5:421–433
40. Nagai Y, Ueno S, Saeki Y, Soga F, Hirano M, Yanagihara T (1996) Decrease of the D3 dopamine receptor mRNA expression in lymphocytes from patients with Parkinson’s disease. Neurology 46:791–795
41. Almanza A, Simon-Arceo K, Coffeen U, Fuentes-Garcia R, Contreras B, Pellicer F, Mercado F (2015) A D2-like receptor family agonist produces analgesia in mechanonociception but not in thermonociception at the spinal cord level in rats. Pharmacol Biochem Behav 137:119–125
42. Taylor BK, Joshi C, Uppal H (2003) Stimulation of dopamine D2 receptors in the nucleus accumbens inhibits inflammatory pain. Brain Res 987:135–143
43. Daginakatte GC, Gadzinski A, Emnett RJ, Stark JL, Gonzales ER, Yan P, Lee JM, Cross AH et al (2008) Expression profiling identifies a molecular signature of reactive astrocytes stimulated by cyclic AMP or proinflammatory cytokines. Exp Neurol 210:261–267
44. Duhen R, Glatigny S, Arbelaez CA, Blair TC, Oukka M, Bettelli E (2013) Cutting edge: the pathogenicity of IFN-gamma-producing Th17 cells is independent of T-bet. J Immunol 190:4478–4482
45. Beaulieu JM, Sotnikova TD, Yao WD, Kockeritz L, Woodgett JR, Gainetdinov RR, Caron MG (2004) Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci U S A 101:5099–5104
46. Nakano K, Higashi T, Hashimoto K, Takagi R, Tanaka Y, Matsushita S (2008) Antagonizing dopamine D1-like receptor inhibits Th17 cell differentiation: preventive and therapeutic effects on experimental autoimmune encephalomyelitis. Biochem Biophys Res Commun 373:286–291
47. Prado C, Contreras F, Gonzalez H, Diaz P, Elgueta D, Barrientos M, Herrada AA, Lladser A et al (2012) Stimulation of dopamine receptor D5 expressed on dendritic cells potentiates Th17-mediated immunity. J Immunol 188:3062–3070
48. Hanami K, Nakano K, Saito K, Okada Y, Yamaoka K, Kubo S, Kondo M, Tanaka Y (2013) Dopamine D2-like receptor signaling suppresses human osteoclastogenesis. Bone 56:1–8
49. Gentile A, Fresegna D, Federici M, Musella A, Rizzo FR, Sepman H, Bullitta S, De Vito F et al (2015) Dopaminergic dysfunction is associated with IL-1beta-dependent mood alterations in experimental autoimmune encephalomyelitis. Neurobiol Dis 74:347–358
50. Hidaka Y, Inaba Y, Matsuda K, Itoh M, Kaneyama T, Nakazawa Y, Koh CS, Ichikawa M (2014) Cytokine production profiles in chronic relapsing-remitting experimental autoimmune encephalomyelitis: IFN-gamma and TNF-alpha are important participants in the first attack but not in the relapse. J Neurol Sci 340:117–122
51. Zorzella-Pezavento SF, Chiuso-Minicucci F, Franca TG, Ishikawa LL, da Rosa LC, Marques C, Ikoma MR, Sartori A (2013) Persistent inflammation in the CNS during chronic EAE despite local absence of IL-17 production. Mediators Inflamm 2013:519627
52. Mastronardi CA, Yu WH, McCann S (2001) Lipopolysaccharide-induced tumor necrosis factor-alpha release is controlled by the central nervous system. Neuroimmunomodulation 9:148–156
53. Fjaer S, Bo L, Myhr KM, Torkildsen O, Wergeland S (2015) Magnetization transfer ratio does not correlate to myelin content in the brain in the MOG-EAE mouse model. Neurochem Int 83–84:28–40
54. Rossi S, Motta C, Studer V, Macchiarulo G, Volpe E, Barbieri F, Ruocco G, Buttari F et al (2014) Interleukin-1beta causes excitotoxic neurodegeneration and multiple sclerosis disease progression by activating the apoptotic protein p53. Mol Neurodegener 9:56
55. Cavallari M, Ceccarelli A, Wang GY, Moscufo N, Hannoun S, Matulis CR, Jackson JS, Glanz BI et al (2014) Microstructural changes in the striatum and their impact on motor and neuropsychological performance in patients with multiple sclerosis. PLoS One 9:e101199
56. Marchi LF, Sesti-Costa R, Ignacchiti MD, Chedraoui-Silva S, Mantovani B (2014) In vitro activation of mouse neutrophils by recombinant human interferon-gamma: increased phagocytosis and release of reactive oxygen species and pro-inflammatory cytokines. Int Immunopharmacol 18:228–235
57. He Y, Du M, Gao Y, Liu H, Wang H, Wu X, Wang Z (2013) Astragaloside IV attenuates experimental autoimmune encephalomyelitis of mice by counteracting oxidative stress at multiple levels. PLoS One 8:e76495
58. Rosenling T, Stoop MP, Attali A, van Aken H, Suidgeest E, Christin C, Stingl C, Suits F et al (2012) Profiling and identification of cerebrospinal fluid proteins in a rat EAE model of multiple sclerosis. J Proteome Res 11:2048–2060
59. Hampe C, Ardila-Osorio H, Fournier M, Brice A, Corti O (2006) Biochemical analysis of Parkinson’s disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum Mol Genet 15:2059–2075
60. Basler M, Mundt S, Muchamuel T, Moll C, Jiang J, Groettrup M, Kirk CJ (2014) Inhibition of the immunoproteasome ameliorates experimental autoimmune encephalomyelitis. EMBO Mol Med 6:226–238
61. George S, Mok SS, Nurjono M, Ayton S, Finkelstein DI, Masters CL, Li QX, Culvenor JG (2010) alpha-Synuclein transgenic mice reveal compensatory increases in Parkinson’s disease-associated proteins DJ-1 and parkin and have enhanced alpha-synuclein and PINK1 levels after rotenone treatment. J Mol Neurosci 42:243–254
62. Petrucelli L, O’Farrell C, Lockhart PJ, Baptista M, Kehoe K, Vink L, Choi P, Wolozin B et al (2002) Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36:1007–1019
63. Lee VM, Trojanowski JQ (2006) Mechanisms of Parkinson’s disease linked to pathological alpha-synuclein: new targets for drug discovery. Neuron 52:33–38
64. Antonelou R, Emmanouilidou E, Gasparinatos G, Velona T, Voumvourakis KI, Stefanis L (2015) Decreased levels of alpha-synuclein in cerebrospinal fluid of patients with clinically isolated syndrome and multiple sclerosis. J Neurochem 134:748–755
65. Marques O, Outeiro TF (2012) Alpha-synuclein: from secretion to dysfunction and death. Cell Death Dis 3:e350
66. Ebrahimi-Fakhari D, Cantuti-Castelvetri I, Fan Z, Rockenstein E, Masliah E, Hyman BT, McLean PJ, Unni VK (2011) Distinct roles in vivo for the ubiquitin-proteasome system and the autophagy-lysosomal pathway in the degradation of alpha-synuclein. J Neurosci 31:14508–14520
67. Bellavista E, Santoro A, Galimberti D, Comi C, Luciani F, Mishto M (2014) Current understanding on the role of standard and immunoproteasomes in inflammatory/immunological pathways of multiple sclerosis. Autoimmune Dis 2014:739705