Age-related Alterations in the Expression of Genes and Synaptic Plasticity Associated with Nitric Oxide Signaling in the Mouse Dorsal Striatum

Overview

Journal Neural Plast

Specialty Neurology

Date 2015 Mar 31

PMID 25821602

Citations 5

Authors

Aisa N Chepkova

Susanne Schonfeld

Olga A Sergeeva

Affiliations

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Abstract

Age-related alterations in the expression of genes and corticostriatal synaptic plasticity were studied in the dorsal striatum of mice of four age groups from young (2-3 months old) to old (18-24 months of age) animals. A significant decrease in transcripts encoding neuronal nitric oxide (NO) synthase and receptors involved in its activation (NR1 subunit of the glutamate NMDA receptor and D1 dopamine receptor) was found in the striatum of old mice using gene array and real-time RT-PCR analysis. The old striatum showed also a significantly higher number of GFAP-expressing astrocytes and an increased expression of astroglial, inflammatory, and oxidative stress markers. Field potential recordings from striatal slices revealed age-related alterations in the magnitude and dynamics of electrically induced long-term depression (LTD) and significant enhancement of electrically induced long-term potentiation in the middle-aged striatum (6-7 and 12-13 months of age). Corticostriatal NO-dependent LTD induced by pharmacological activation of group I metabotropic glutamate receptors underwent significant reduction with aging and could be restored by inhibition of cGMP hydrolysis indicating that its age-related deficit is caused by an altered NO-cGMP signaling cascade. It is suggested that age-related alterations in corticostriatal synaptic plasticity may result from functional alterations in receptor-activated signaling cascades associated with increasing neuroinflammation and a prooxidant state.

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References

Cai H . NAD(P)H oxidase-dependent self-propagation of hydrogen peroxide and vascular disease. Circ Res. 2005; 96(8):818-22. DOI: 10.1161/01.RES.0000163631.07205.fb. View

Sammut S, Threlfell S, West A . Nitric oxide-soluble guanylyl cyclase signaling regulates corticostriatal transmission and short-term synaptic plasticity of striatal projection neurons recorded in vivo. Neuropharmacology. 2009; 58(3):624-31. PMC: 2813362. DOI: 10.1016/j.neuropharm.2009.11.011. View

Cepeda C, Li Z, Levine M . Aging reduces neostriatal responsiveness to N-methyl-D-aspartate and dopamine: an in vitro electrophysiological study. Neuroscience. 1996; 73(3):733-50. DOI: 10.1016/0306-4522(96)00056-5. View

Akopian G, Walsh J . Pre- and postsynaptic contributions to age-related alterations in corticostriatal synaptic plasticity. Synapse. 2006; 60(3):223-38. DOI: 10.1002/syn.20289. View

Tadros S, DSouza M, Zhu X, Frisina R . Gene expression changes for antioxidants pathways in the mouse cochlea: relations to age-related hearing deficits. PLoS One. 2014; 9(2):e90279. PMC: 3938674. DOI: 10.1371/journal.pone.0090279. View

Gerdeman G, Ronesi J, Lovinger D . Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci. 2002; 5(5):446-51. DOI: 10.1038/nn832. View

Marchand W, Lee J, Suchy Y, Garn C, Johnson S, Wood N . Age-related changes of the functional architecture of the cortico-basal ganglia circuitry during motor task execution. Neuroimage. 2010; 55(1):194-203. DOI: 10.1016/j.neuroimage.2010.12.030. View

Jha M, Lee S, Park D, Kook H, Park K, Lee I . Diverse functional roles of lipocalin-2 in the central nervous system. Neurosci Biobehav Rev. 2014; 49:135-56. DOI: 10.1016/j.neubiorev.2014.12.006. View

Dalbem A, Silveira C, Pedroso M, Vaz Breda R, Baes C, Bartmann A . Altered distribution of striatal activity-dependent synaptic plasticity in the 3-nitropropionic acid model of Huntington's disease. Brain Res. 2005; 1047(2):148-58. DOI: 10.1016/j.brainres.2005.04.030. View

10.

West A, Tseng K . Nitric Oxide-Soluble Guanylyl Cyclase-Cyclic GMP Signaling in the Striatum: New Targets for the Treatment of Parkinson's Disease?. Front Syst Neurosci. 2011; 5:55. PMC: 3129139. DOI: 10.3389/fnsys.2011.00055. View

11.

Floyd R, Hensley K . Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiol Aging. 2002; 23(5):795-807. DOI: 10.1016/s0197-4580(02)00019-2. View

12.

Wang Y . Differential effect of aging on synaptic plasticity in the ventral and dorsal striatum. Neurobiol Learn Mem. 2007; 89(1):70-5. DOI: 10.1016/j.nlm.2007.08.015. View

13.

Mariani E, Polidori M, Cherubini A, Mecocci P . Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J Chromatogr B Analyt Technol Biomed Life Sci. 2005; 827(1):65-75. DOI: 10.1016/j.jchromb.2005.04.023. View

14.

Tozzi A, Costa C, Siliquini S, Tantucci M, Picconi B, Kurz A . Mechanisms underlying altered striatal synaptic plasticity in old A53T-α synuclein overexpressing mice. Neurobiol Aging. 2011; 33(8):1792-9. DOI: 10.1016/j.neurobiolaging.2011.05.002. View

15.

Wardas J, Pietraszek M, Schulze G, Ossowska K, Wolfarth S . Age-related changes in glutamate receptors: an autoradiographic analysis. Pol J Pharmacol. 1998; 49(6):401-10. View

16.

Gorin Y, Block K . Nox as a target for diabetic complications. Clin Sci (Lond). 2013; 125(8):361-82. DOI: 10.1042/CS20130065. View

17.

Chepkova A, Selbach O, Haas H, Sergeeva O . Ammonia-induced deficit in corticostriatal long-term depression and its amelioration by zaprinast. J Neurochem. 2012; 122(3):545-56. DOI: 10.1111/j.1471-4159.2012.07806.x. View

18.

Domek-Lopacinska K, van de Waarenburg M, Markerink-van Ittersum M, Steinbusch H, de Vente J . Nitric oxide-induced cGMP synthesis in the cholinergic system during the development and aging of the rat brain. Brain Res Dev Brain Res. 2005; 158(1-2):72-81. DOI: 10.1016/j.devbrainres.2005.06.003. View

19.

Mancini M, Ricci A, Zaccheo D, Amenta F . Similarity of age-dependent changes in renal and striatal dopamine receptors. Funct Neurol. 1991; 6(3):227-9. View

20.

Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M . A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci. 1999; 19(7):2489-99. PMC: 6786075. View