Advertisement

β-Amyloid 25–35 Suppresses the Secretory Activity of the Dopaminergic System in the Rat Brain

  • V. N. MukhinEmail author
  • V. V. Sizov
  • K. I. Pavlov
  • V. M. Klimenko
Article

Dysfunction of the dopaminergic system of the brain may underlie a number of the clinical manifestations of Alzheimer’s disease. Published data provide evidence that impairments to the normal metabolism of β-amyloid may be the cause of such dysfunction. Experimental increases in β-amyloid levels in the brains of animals lead to decreases in the extracellular dopamine levels and its long-term (tonic) changes in the dorsal ventral striatum. The aim of the present work was to study the effects of β-amyloid on short-term (phasic) changes in dopamine secretion. Aggregated β-amyloid (25–35) solution or physiological saline was administered into the ventricular system of the brains of urethane-anesthetized rats. Dopamine release induced by electrical stimulation was recorded before administration and 10, 30, and 60 min after administration by fast-scan cyclic voltammetry. Dopamine release in the dorsomedial striatum was decreased during the first hour after β-amyloid administration. No statistically significant changes in the core and shell of the nucleus accumbens were seen.

Keywords

Alzheimer’s disease dopamine β-amyloid fast-scan cyclic voltammetry 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    S. A. Litvinova, P. M. Klodt, V. S. Kudrin, et al., “Studies of behavior and neurotransmitter content in brain structures in rats with a model of Alzheimer’s disease based on administration of β-amyloid 25–35,” Neirokhimiya, 32, No. 1, 48 (2015).Google Scholar
  2. 2.
    V. N. Mukhin, “Pathogenetic mechanisms of dysfunction of the basal cholinergic system in Alzheimer’s disease,” Ros. Fiziol. Zh., 99, No. 7, 793–804 (2013).Google Scholar
  3. 3.
    V. N. Mukhin and V. M. Klimenko, “Mechanisms of impairments to long-term potentiation in Alzheimer’s disease,” Med. Akad. Zh., 14, No. 1, 42–51 (2014).Google Scholar
  4. 4.
    P. Allard, I. Alafuzoff, A. Carlsson, et al., “Loss of dopamine uptake sites labeled with GBR-12935 in Alzheimer’s disease,” Eur. Neurology, 30, No. 4, 181–185 (1990).Google Scholar
  5. 5.
    O. Ambrée, H. Richter, N. Sachser, et al., “Levodopa ameliorates learning and memory deficits in a murine model of Alzheimer’s disease,” Neurobiol. Aging, 30, No. 8, 1192–1204 (2009).Google Scholar
  6. 6.
    H. Aral, K. Kosaka, and R. Iizuka, “Changes of biogenic amines and their metabolites in postmortem brains from patients with Alzheimertype dementia,” J. Neurochem., 43, No. 2, 388–393 (1984).Google Scholar
  7. 7.
    S. Arold, P. Sullivan, T. Bilousova, et al., “Apolipoprotein E level and cholesterol are associated with reduced synaptic amyloid beta in Alzheimer’s disease and apoE TR mouse cortex,” Acta Neuropathol., 123, No. 1, 39–52 (2012).Google Scholar
  8. 8.
    J. R. Brorson, V. P. Bindokas, T. Iwama, et al., “The Ca2+ influx induced by β-amyloid peptide 25–35 in cultured hippocampal neurons results from network excitation,” J. Neurobiol., 26, No. 3, 325–338 (1995).Google Scholar
  9. 9.
    E. A. Budygin, M. R. Kilpatrick, R. R. Gainetdinov, and R. M. Wightman, “Correlation between behavior and extracellular dopamine levels in rat striatum: comparison of microdialysis and fast-scan cyclic voltammetry,” Neurosci. Lett., 281, No. 1, 9–12 (2000).Google Scholar
  10. 10.
    J. Busciglio, D. H. Gabuzda, P. Matsudaira, and B. A. Yankner, “Generation of beta-amyloid in the secretory pathway in neuronal and nonneuronal cells,” Proc. Natl. Acad. Sci. USA, 90, No. 5, 2092–2096 (1993).Google Scholar
  11. 11.
    Z. Chang, Y. Luo, Y. Zhang, and G. Wei, “Interactions of Aβ25–35 β-barrel-like oligomers with anionic lipid bilayer and resulting membrane leakage: An all-atom molecular dynamics study,” J. Phys. Chem. B, 115, No. 5, 1165–1174 (2011).Google Scholar
  12. 12.
    J. R. Cirrito, K. A. Yamada, M. B. Finn, et al., “Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo,” Neuron, 48, No. 6, 913–922 (2005).Google Scholar
  13. 13.
    A. J. Cross, T. J. Crow, I. N. Ferrier, et al., “Striatal dopamine receptors in Alzheimer-type dementia,” Neurosci. Lett., 52, No. 1–2, 1–6 (1984).Google Scholar
  14. 14.
    S. Delobette, A. Privat, and T. Maurice, “In vitro aggregation facilities beta-amyloid peptide-(25–35)-induced amnesia in the rat,” Eur. J. Pharmacol., 319, No. 1, 1–4 (1997).Google Scholar
  15. 15.
    C. Duyckaerts, B. Delatour, and M.-C. Potier, “Classification and basic pathology of Alzheimer disease,” Acta Neuropathol., 118, No. 1, 5–36 (2009).Google Scholar
  16. 16.
    N. Eshel, J. Tian, and N. Uchida, “Opening the black box: dopamine, predictions, and learning,” Trends Cogn. Sci., 17, No. 9, 430–431 (2013).Google Scholar
  17. 17.
    D. B. Freir, C. Holscher, and C. E. Herron, “Blockade of long-term potentiation by beta-amyloid peptides in the CA1 region of the rat hippocampus in vivo,” J. Neurophysiol., 85, No. 2, 708–713 (2001).Google Scholar
  18. 18.
    P. A. Garris and R. M. Wightman, “Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study,” J. Neurosci., 14, No. 1, 442–450 (1994).Google Scholar
  19. 19.
    S. Gengler, V. A. Gault, P. Harriott, and C. Hölscher, “Impairments of hippocampal synaptic plasticity induced by aggregated beta-amyloid (25–35) are dependent on stimulation-protocol and genetic background,” Exp. Brain Res., 179, No. 4, 621–630 (2007).Google Scholar
  20. 20.
    K. Guzmán-Ramos, P. Moreno-Castilla, M. Castro-Cruz, et al., “Restoration of dopamine release deficits during object recognition memory acquisition attenuates cognitive impairment in a triple transgenic mice model of Alzheimer’s disease,” Learn. Mem., 19, No. 10, 453–460 (2012).Google Scholar
  21. 21.
    K. Hensley, J. M. Carney, M. P. Mattson, et al., “A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease,” Proc. Natl. Acad. Sci. USA, 91, No. 8, 3270–3274 (1994).Google Scholar
  22. 22.
    T. Hochstrasser, L. A. Hohsfield, B. Sperner-Unterweger, and C. Humpel, “β-Amyloid induced effects on cholinergic, serotonergic, and dopaminergic neurons is differentially counteracted by anti-inflammatory drugs,” J. Neurosci. Res., 91, No. 1, 83–94 (2013).Google Scholar
  23. 23.
    J. Horvath, P. R. Burkhard, F. R. Herrmann, et al., “Neuropathology of parkinsonism in patients with pure Alzheimer’s disease,” J. Alzheimers Dis., 39, No. 1, 115–120 (2014).Google Scholar
  24. 24.
    A. Itoh, A. Nitta, M. Nadai, et al., “Dysfunction of cholinergic and dopaminergic neuronal systems in beta-amyloid protein-infused rats,” J. Neurochem., 66, No. 3, 1113–1117 (1996).Google Scholar
  25. 25.
    S. R. Jones, T. A. Mathews, and E. A. Budygin, “Effect of moderate ethanol dose on dopamine uptake in rat nucleus accumbens in vivo,” Synapse, 60, No. 3, 251–255 (2006).Google Scholar
  26. 26.
    F. Kamenetz, T. Tomita, H. Hsieh, et al., “APP processing and synaptic function,” Neuron, 37, No. 6, 925–937 (2003).Google Scholar
  27. 27.
    Y. G. Kaminsky, M. W. Marlatt, M. A. Smith, and E. A. Kosenko, “Subcellular and metabolic examination of amyloid-β peptides in Alzheimer disease pathogenesis: Evidence for Aβ25–35,” Exper. Neurology, 221, No. 1, 26–37 (2010).Google Scholar
  28. 28.
    E. Karran and B. De Strooper, “The amyloid cascade hypothesis: are we poised for success or failure?” J. Neurochem., 139, 237–252 (2016).Google Scholar
  29. 29.
    N. Kemppainen, M. Laine, M. P. Laakso, et al., “Hippocampal dopamine D2 receptors correlate with memory functions in Alzheimer’s disease,” Eur. J. Neurosci., 18, No. 1, 149–154 (2003).Google Scholar
  30. 30.
    S. Kemppainen, P. Lindholm, E. Galli, et al., “Cerebral dopamine neurotrophic factor improves long-term memory in APP/PS1 transgenic mice modeling Alzheimer’s disease as well as in wild-type mice,” Behav. Brain Res., 291, 1–11 (2015).Google Scholar
  31. 31.
    G. Koch, F. Di Lorenzo, S. Bonni, et al., “Dopaminergic modulation of cortical plasticity in Alzheimer’s disease patients,” Neuropsychophar macology, 39, No. 11, 2654–2661 (2014).Google Scholar
  32. 32.
    A. R. Koudinov and N. V. Koudinova, “Alzheimer’s soluble amyloid beta protein is secreted by HepG2 cells as an apolipoprotein,” Cell Biol. Int., 21, No. 5, 265–271 (1997).Google Scholar
  33. 33.
    T. Kubo, Y. Kumagae, C. A. Miller, and I. Kaneko, “β-Amyloid racemized at the Ser26 residue in the brains of patients with Alzheimer disease: implications in the pathogenesis of Alzheimer disease,” J. Neuropathol. Exp. Neurol., 62, No. 3, 248–259 (2003).Google Scholar
  34. 34.
    U. Kumar and S. C. Patel, “Immunohistochemical localization of dopamine receptor subtypes (D1R–D5R) in Alzheimer’s disease brain,” Brain Res., 1131, 187–196 (2007).Google Scholar
  35. 35.
    A. Martorana, F. Di Lorenzo, Z. Esposito, et al., “Dopamine D2-agonist Rotigotine effects on cortical excitability and central cholinergic transmission in Alzheimer’s disease patients,” Neuropharmacology, 64, 108–113 (2013).Google Scholar
  36. 36.
    A. Martorana and G. Koch, “Is dopamine involved in Alzheimer’s disease?” Front. Aging Neurosci., 6, 252 (2014).Google Scholar
  37. 37.
    A. Martorana, F. Mori, Z. Esposito, et al., “Dopamine modulates cholinergic cortical excitability in Alzheimer’s disease patients,” Neuropsychopharmacology, 34, No. 10, 2323–2328 (2009).Google Scholar
  38. 38.
    L. Millucci, L. Ghezzi, G. Bernardini, and A. Santucci, “Conformations and biological activities of amyloid beta peptide 25–35,” Curr. Protein Pept. Sci., 11, No. 1, 54–67 (2010).Google Scholar
  39. 39.
    R. A. Mitchell, N. Herrmann, and K. L. Lanctot, “The role of dopamine in symptoms and treatment of apathy in Alzheimer’s disease,” CNS Neurosci. Therap., 17, No. 5, 411–427 (2011).Google Scholar
  40. 40.
    P. Moreno-Castilla, L. F. Rodriguez-Duran, K. Guzman-Ramos, et al., “Dopaminergic neurotransmission dysfunction induced by amyloid-β transforms cortical long-term potentiation into long-term depression and produces memory impairment,” Neurobiol. Aging, 41, 187–199 (2016).Google Scholar
  41. 41.
    A. M. Murray, F. B. Weihmueller, J. F. Marshall, et al., “Damage to dopamine systems differs between Parkinson’s disease and Alzheimer’s disease with parkinsonism,” Ann. Neurol., 37, No. 3, 300–312 (1995).Google Scholar
  42. 42.
    A. J. Nazarali and G. P. Reynolds, “Monoamine neurotransmitters and their metabolites in brain regions in Alzheimer’s disease: A postmortem study,” Cell. Mol. Neurobiol., 12, No. 6, 581–587 (1992).Google Scholar
  43. 43.
    A. Nobili, E. C. Latagliata, M. T. Viscomi, et al., “Dopamine neuronal loss contributes to memory and reward dysfunction in a model of Alzheimer’s disease,” Nat. Commun., 8, 14727 (2017).Google Scholar
  44. 44.
    E. B. Oleson, J. Salek, K. D. Bonin, et al., “Real-time voltammetric detection of cocaine-induced dopamine changes in the striatum of freely moving mice,” Neurosci. Lett., 467, No. 2, 144–146 (2009).Google Scholar
  45. 45.
    J. J. Palop and L. Mucke, “Amyloid-β-induced neuronal dysfunction in Alzheimer’s disease: from synapses toward neural networks,” Nature Neurosci., 13, No. 7, 812–818 (2010).Google Scholar
  46. 46.
    M. S. Parihar and G. J. Brewer, “Amyloid beta as a modulator of synaptic plasticity,” J. Alzheimers Dis., 22, No. 3, 741–763 (2010).Google Scholar
  47. 47.
    S. E. Perez, O. Lazarov, J. B. Koprich, et al., “Nigrostriatal dysfunction in familial Alzheimer’s disease-linked APPswe/PS1AE9 transgenic mice,” J. Neurosci., 25, No. 44, 10220–10229 (2005).Google Scholar
  48. 48.
    C. J. Pike, D. Burdick, A. J. Walencewicz, et al., “Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state,” J. Neurosci., 13, No. 4, 1676–1687 (1993).Google Scholar
  49. 49.
    G. Pizzolato, F. Chierichetti, M. Fabbri, et al., “Reduced striatal dopamine receptors in Alzheimer’s disease Single photon emission tomography study with the D sub 2 tracer -IBZM,” Neurology, 47, No. 4, 1065–1068 (1996).Google Scholar
  50. 50.
    S. Preda, S. Govoni, C. Lanni, et al., “Acute β-amyloid administration disrupts the cholinergic control of dopamine release in the nucleus accumbens,” Neuropsychopharmacology, 33, No. 5, 1062–1070 (2007).Google Scholar
  51. 51.
    K. J. Reinikainen, L. Paljarvi, T. Halonen, et al., “Dopaminergic system and monoamine oxidase-β activity in Alzheimer’s disease,” Neurobiol. Aging, 9, 245–252 (1988).Google Scholar
  52. 52.
    J. O. Rinne, E. Sako, L. Paljarvi, et al., “Brain dopamine D-2 receptors n senile dementia,” J. Neural Transm., 65, No. 1, 51–62 (1986).Google Scholar
  53. 53.
    P. H. Robert, E. Mulin, P. Malléa, and R. David, “REVIEW: Apathy diagnosis, assessment, and treatment in Alzheimer’s disease,” CNS Neurosci. Therap., 16, No. 5, 263–271 (2010).Google Scholar
  54. 54.
    N. T. Rodeberg, J. A. Johnson, C. M. Cameron, et al., “Construction of training sets for valid calibration of in vivo cyclic voltammetric data by principal component analysis,” Anal. Chem., 87, No. 22, 11484–11491 (2015).Google Scholar
  55. 55.
    C. Rovira, N. Arbez, and J. Mariani, “Abeta(25–35) and Abeta(1–40) act on different calcium channels in CA1 hippocampal neurons,” Biochem. Biophys. Res. Commun, 296, No. 5, 1317–1321 (2002).Google Scholar
  56. 56.
    M. Sawada, Y. Hirata, H. Arai, et al., “Tyrosine hydroxylase, tryptophan hydroxylase, biopterin, and neopterin in the brains of normal controls and patients with senile dementia of Alzheimer type,” J. Neurochem., 48, No. 3, 760–764 (1987).Google Scholar
  57. 57.
    G. Simic, M. Babic Leko, S. Wray, et al., “Monoaminergic neuropathology in Alzheimer’s disease,” Progr. Neurobiol., 151, 101–138 (2017).Google Scholar
  58. 58.
    S. E. Starkstein, G. Petracca, E. Chemerinski, and J. Kremer, “Syndromic validity of apathy in Alzheimer’s disease,” Am. J. Psychiatry, 158, No. 6, 872–877 (2001).Google Scholar
  59. 59.
    E. E. Steinberg, R. Keifl in, J. R. Boivin, et al., “A causal link between prediction errors, dopamine neurons and learning,” Nat. Neurosci., 16, No. 7, 966–973 (2013).Google Scholar
  60. 60.
    D. Storga, K. Vrecko, J. G. D. Birkmayer, and G. Reibnegger, “Monoaminergic neurotransmitters, their precursors and metabolites in brains of Alzheimer patients,” Neurosci. Lett., 203, No. 1, 29–32 (1996).Google Scholar
  61. 61.
    R. A. Sweet, R. L. Hamilton, M. T. Healy, et al., “Alterations of striatal dopamine receptor binding in Alzheimer disease are associated with Lewy body pathology and antemortem psychosis,” Arch. Neurol., 58, No. 3, 466–472 (2001).Google Scholar
  62. 62.
    Y. Tanaka, K. Meguro, S. Yamaguchi, et al., “Decreased striatal D2 receptor density associated with severe behavioral abnormality in Alzheimer’s disease,” Ann. Nucl. Med., 17, No. 7, 567–573 (2003).Google Scholar
  63. 63.
    P. N. Tariot, R. M. Cohen, T. Sunderland, et al., “L-deprenyl in Alzheimer’s disease. Preliminary evidence for behavioral change with monoamine oxidase B inhibition,” Arch. Gen. Psych., 44, No. 5, 427–433 (1987).Google Scholar
  64. 64.
    L. Trillo, D. Das, W. Hsieh, et al., “Ascending monoaminergic systems alterations in Alzheimer’s disease. Translating basic science into clinical care,” Neurosci. Biobehav. Rev., 37, No. 8, 1363–1379 (2013).Google Scholar
  65. 65.
    S. S. Uzakov, A. D. Ivanov, S. V. Salozhin, et al., “Lentiviralmediated overexpression of nerve growth factor (NGF) prevents beta-amyloid -induced long term potentiation (LTP) decline in the rat hippocampus,” Brain Res., 1624, 398–404 (2015).Google Scholar
  66. 66.
    D. Wang, Y. Noda, Y. Zhou, et al., “The allosteric potentiation of nicotinic acetylcholine receptors by galantamine ameliorates the cognitive dysfunction in beta amyloid 25–35 i.c.v.-injected mice: Involvement of dopaminergic systems,” Neuropsychopharmacology, 32, No. 6, 1261–1271 (2006).Google Scholar
  67. 67.
    Y. Wang, L. Liu, W. Hu, and G. Li, “Mechanism of soluble beta-amyloid 25–35 neurotoxicity in primary cultured rat cortical neurons,” Neurosci. Lett., 618, 72–76 (2016).Google Scholar
  68. 68.
    W. Wei, L. N. Nguyen, H. W. Kessels, et al., “Amyloid beta from axons and dendrites reduces local spine number and plasticity,” Nature Neurosci., 13, No. 2, 190–196 (2010).Google Scholar
  69. 69.
    P. Xu, Z. Li, H. Wang, et al., “Triptolide inhibited cytotoxicity of differentiated PC12 cells induced by amyloid-beta25–35 via the autophagy pathway,” PLoS One, 10, No. 11, e0142719 (2015).Google Scholar
  70. 70.
    H. Yang and A. C. Michael, “In vivo fast-scan cyclic voltammetry of dopamine near microdialysis probes,” in: Electrochemical Methods for Neuroscience, A. C. Michael and L. M. Borland (eds.), CRC Press, Boca Raton (2007).Google Scholar
  71. 71.
    B. A. Yankner, L. K. Duffy, and D. A. Kirschner, “Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides,” Science, 250, No. 4978, 279–282 (1990).Google Scholar
  72. 72.
    C. M. Yates, J. Simpson, A. Gordon, et al., “Catecholamines and cholinergic enzymes in pre-senile and senile Alzheimer-type dementia and Down’s syndrome,” Brain Res., 280, No. 1, 119–126 (1983).Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • V. N. Mukhin
    • 1
    Email author
  • V. V. Sizov
    • 1
  • K. I. Pavlov
    • 1
  • V. M. Klimenko
    • 1
  1. 1.Institute of Experimental MedicineSt. PetersburgRussia

Personalised recommendations