Neuropeptide-S affects cognitive impairment and depression-like behavior on MPTP induced experimental mouse model of Parkinson’s disease

Neuropeptide-S affects cognitive impairment and depression-like behavior on MPTP induced experimental mouse model of Parkinson’s disease

Background/aim: The present study proposes to investigate the effect of neuropeptide–S (NPS) on cognitive functions and depressionlike behavior of MPTP-induced experimental model of Parkinson’s disease (PD). Materials and methods: Three-month-old C57BL/6 mice were randomly divided into three groups as; Control, Methyl-4-phenyl1,2,3,6-tetrahydropyridine (MPTP) and MPTP + NPS 0.1 nmol (received intraperitoneal injection of MPTP and intracerebroventricular injection of NPS, 0.1 nmol for seven days). The radial arm maze and pole tests were carried out, and the levels of tyrosine hydroxylase (TH) were determined using western blotting. A mass spectrometer was used to measure the levels of dopamine, glutamic acid, and glutamine. Results: The T-turn and time to descend enhanced in MPTP group, while these parameters were decreased by NPS treatment. In the MPTP group, the number of working memory errors (WME) and reference memory errors (RME) increased, whereas NPS administration decreased both parameters. Sucrose preference decreased in the MPTP group while increasing in the NPS group. MPTP injection significantly reduced dopamine, glutamic acid, and glutamine levels. NPS treatment restored the MPTP-induced reduction in glutamine and glutamic acid levels. Conclusion: NPS may be involved in the future treatment of cognitive impairments and depression-like behaviors in PD.Key words: Parkinson’s disease, neuropeptide-S, cognition, depression-like behavior

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  • 1. Sveinbjornsdottir S. The clinical symptoms of Parkinson’s disease. Journal of Neurochemistry 2016; 139: 318-324. doi: 10.1111/jnc.13691
  • 2. Tysnes OB, Storstein A. Epidemiology of Parkinson’s disease. Journal of Neural Transmission 2017; 124 (8): 901-905. doi: 10.1007/s00702-017-1686-y
  • 3. Ziemssen T, Reichmann H. Non-motor dysfunction in Parkinson’s disease. Parkinsonism & Related Disorders 2007; 13 (6): 323-332. doi: 10.1016/j.parkreldis.2006.12.014
  • 4. Tadaiesky MT, Dombrowski PA, Figueiredo CP, CargninFerreira E, Da Cunha C et al. Emotional, cognitive and neurochemical alterations in a premotor stage model of Parkinson’s disease. Neuroscience 2008; 156 (4): 830-840. doi: 10.1016/j.neuroscience.2008.08.035
  • 5. Litvan I, Aarsland D, Adler CH, Goldman JG, Kulisevsky J et al. MDS Task Force on mild cognitive impairment in Parkinson’s disease: critical review of PD-MCI. Movement Disorders 2011; 26 (10): 1814-1824. doi: 10.1002/mds.23823
  • 6. Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG. The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Movement Disorders 2008; 23 (6): 837- 844. doi: 10.1002/mds.21956
  • 7. Tolosa E, Compta Y, Gaig C. The premotor phase of Parkinson’s disease. Parkinsonism & Related Disorders 2007; 13: Supplement S2-S7. doi: 10.1016/j.parkreldis.2007.06.007
  • 8. Mattila PM, Rinne JO, Helenius H, Roytta M. Neuritic degeneration in the hippocampus and amygdala in Parkinson’s disease in relation to Alzheimer pathology. Acta Neuropathologica 1999; 98 (2): 157-164. doi: 10.1007/ s004010051064
  • 9. Mally J, Szalai G, Stone TW. Changes in the concentration of amino acids in serum and cerebrospinal fluid of patients with Parkinson’s disease. Journal of the Neurological Sciences 1997; 151 (2): 159-162. doi: 10.1016/s0022-510x(97)00119-6
  • 10. Ho YJ, Ho SC, Pawlak CR, Yeh KY. Effects of D-cycloserine on MPTP-induced behavioral and neurological changes: potential for treatment of Parkinson’s disease dementia. Behavioral Brain Research 2011; 219 (2): 280-290. doi: 10.1016/j.bbr.2011.01.028
  • 11. O’Gorman Tuura RL, Baumann CR, Baumann-Vogel H. Beyond Dopamine: GABA, glutamate, and the axial symptoms of Parkinson Disease. Frontiers in Neurology 2018; (9): 806. doi: 10.3389/fneur.2018.00806
  • 12. Przedborski S, Tieu K, Perier C, Vila M. MPTP as a mitochondrial neurotoxic model of Parkinson’s disease. Journal of Bioenergetics and Biomembranes 2004; 36 (4): 375-379. doi: 10.1023/B:JOBB.0000041771.66775.d5
  • 13. Vuckovic MG, Wood RI, Holschneider DP, Abernathy A, Togasaki DM et al. Memory, mood, dopamine, and serotonin in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. Neurobiology of Disease 2008; 32 (2): 319-327. doi: 10.1016/j.nbd.2008.07.015
  • 14. Crabbe M, Van der Perren A, Weerasekera A, Himmelreich U, Baekelandt V et al. Altered mGluR5 binding potential and glutamine concentration in the 6-OHDA rat model of acute Parkinson’s disease and levodopa-induced dyskinesia. Neurobiol Aging 2018; 61: 82-92. doi: 10.1016/j.neurobiolaging.2017.09.006
  • 15. Xu YL, Reinscheid RK, Huitron-Resendiz S, Clark SD, Wang Z et al. Neuropeptide S: a neuropeptide promoting arousal and anxiolytic-like effects. Neuron 2004; 43 (4): 487-497. doi: 10.1016/j.neuron.2004.08.005
  • 16. Reinscheid RK, Xu YL. Neuropeptide S as a novel arousal promoting peptide transmitter. The FEBS Journal 2005; 272 (22): 5689-5693. doi: 10.1111/j.1742-4658.2005.04982.x
  • 17. Xu YL, Gall CM, Jackson VR, Civelli O, Reinscheid RK. Distribution of neuropeptide S receptor mRNA and neurochemical characteristics of neuropeptide S-expressing neurons in the rat brain. The Journal of Comparative Neurology 2007; 500 (1): 84-102. doi: 10.1002/cne.21159
  • 18. Zhang Y, Wang Z, Parks GS, Civelli O. Novel neuropeptides as ligands of orphan G protein-coupled receptors. Current Pharmaceutical Design 2011; 17 (25): 2626-2631. doi: 10.2174/138161211797416110
  • 19. Reinscheid RK, Xu YL, Okamura N, Zeng J, Chung S et al. Pharmacological characterization of human and murine neuropeptide s receptor variants. The Journal of Pharmacology Experimental Therapeutics 2005; 315 (3): 1338-1345. doi: 10.1124/jpet.105.093427
  • 20. Reinscheid RK, Xu YL. Neuropeptide S and its receptor: a newly deorphanized G protein-coupled receptor system. Neuroscientist 2005; 11 (6): 532-538. doi: 10.1177/1073858405276405
  • 21. Beck B, Fernette B, Stricker-Krongrad A. Peptide S is a novel potent inhibitor of voluntary and fast-induced food intake in rats. Biochemical and Biophysical Research Communications 2005; 332 (3): 859-865. doi: 10.1016/j.bbrc.2005.05.029
  • 22. Smith KL, Patterson M, Dhillo WS, Patel SR, Semjonous NM et al. Neuropeptide S stimulates the hypothalamo-pituitaryadrenal axis and inhibits food intake. Endocrinology 2006; 147 (7): 3510-3518. doi: 10.1210/en.2005-1280
  • 23. Pape HC, Jungling K, Seidenbecher T, Lesting J, Reinscheid RK. Neuropeptide S: a transmitter system in the brain regulating fear and anxiety. Neuropharmacology 2010; 58 (1): 29-34. doi: 10.1016/j.neuropharm.2009.06.001
  • 24. Okamura N, Garau C, Duangdao DM, Clark SD, Jungling K et al. Neuropeptide S enhances memory during the consolidation phase and interacts with noradrenergic systems in the brain. Neuropsychopharmacology 2011; 36 (4): 744-752. doi: 10.1038/npp.2010.207
  • 25. Zhao P, Qian X, Nie Y, Sun N, Wang Z et al. Neuropeptide S ameliorates cognitive impairment of APP/PS1 transgenic mice by promoting synaptic plasticity and reducing Aβ deposition. Frontiers in Behavioral Neuroscience 2019; 13: 138. doi: 10.3389/fnbeh.2019.00138
  • 26. Aras S, Tanriover G, Aslan M, Yargicoglu P, Agar A. The role of nitric oxide on visual-evoked potentials in MPTP-induced Parkinsonism in mice. Neurochemistry International 2014; 72: 48-57. doi: 10.1016/j.neuint.2014.04.014
  • 27. Sunter D, Hewson AK, Dickson SL. Intracerebroventricular injection of apelin-13 reduces food intake in the rat. Neuroscience Letters 2003; 353 (1): 1-4. doi: 10.1016/s0304- 3940(03)00351-3
  • 28. Ozkan A, Parlak H, Tanriover G, Dilmac S, Ulker SN et al. The protective mechanism of docosahexaenoic acid in mouse model of Parkinson: The role of hemeoxygenase. Neurochemistry International 2016; 101: 110-119. doi: 10.1016/j.neuint.2016.10.012
  • 29. Moorthi P, Premkumar P, Priyanka R, Jayachandran KS, Anusuyadevi M. Pathological changes in hippocampal neuronal circuits underlie age-associated neurodegeneration and memory loss: positive clue toward SAD. Neuroscience 2015; 301: 90-105. doi: 10.1016/j.neuroscience.2015.05.062
  • 30. Liu MY, Yin CY, Zhu LJ, Zhu XH, Xu C et al. Sucrose preference test for measurement of stress-induced anhedonia in mice. Nature Protocols 2018; 13 (7): 1686-1698. doi: 10.1038/s41596- 018-0011-z
  • 31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976; 72: 248-254. doi: 10.1006/abio.1976.9999
  • 32. Gonzalez RR, Fernandez RF, Vidal JL, Frenich AG, Perez ML. Development and validation of an ultra-high performance liquid chromatography-tandem mass-spectrometry (UHPLCMS/MS) method for the simultaneous determination of neurotransmitters in rat brain samples. Journal of Neuroscience Methods 2011; 198 (2): 187-194. doi: 10.1016/j. jneumeth.2011.03.023
  • 33. Bülbül M, Sinen O, Özkan A, Aslan MA, Ağar A. Central neuropeptide-S treatment improves neurofunctions of 6-OHDA-induced Parkinsonian rats. Experimental Neurology 2019; 317: 78-86. doi: 10.1016/j.expneurol.2019.02.015
  • 34. Bohlen OV. Modeling neurodegenerative diseases in vivo review. Neurodegenerative Diseases 2006; 2 (6): 313-320. doi: 10.1159/000092318
  • 35. Langston JW. The MPTP story. Journal of Parkinson’s Disease 2017; 7 (Supplement 1): S11-S19. doi: 10.3233/JPD-179006
  • 36. Sedelis M, Hofele K, Auburger GW, Morgan S, Huston JP et al. MPTP susceptibility in the mouse: behavioral, neurochemical, and histological analysis of gender and strain differences. Behavior Genetics 2000; 30 (3): 171-182. doi: 10.1023/a:1001958023096
  • 37. Okamura N, Reinscheid RK. Neuropeptide S: a novel modulator of stress and arousal. Stress 2007; 10 (3): 221-226. doi: 10.1080/10253890701248673
  • 38. White RB, Thomas MG. Moving beyond tyrosine hydroxylase to define dopaminergic neurons for use in cell replacement therapies for Parkinson’s disease. CNS Neurological Disorders Drug Targets 2012; 11 (4): 340-349. doi: 10.2174/187152712800792758
  • 39. Park HJ, Lim S, Joo WS, Yin CS, Lee HS et al. Acupuncture prevents 6-hydroxydopamine-induced neuronal death in the nigrostriatal dopaminergic system in the rat Parkinson’s disease model. Experimental Neurology 2003; 180 (1): 93-98. doi: 10.1016/s0014-4886(02)00031-6
  • 40. Zhu G, Chen Y, Huang Y, Li Q, Behnisch T. MPTP-meditated hippocampal dopamine deprivation modulates synaptic transmission and activity-dependent synaptic plasticity. Toxicology and Applied Pharmacology 2011; 254 (3): 332-341. doi: 10.1016/j.taap.2011.05.007
  • 41. Meis S, Bergado-Acosta JR, Yanagawa Y, Obata K, Stork O et al. Identification of a neuropeptide S responsive circuitry shaping amygdala activity via the endopiriform nucleus. PLoS One 2008; 3 (7): e2695. doi: 10.1371/journal.pone.0002695
  • 42. Jungling K, Seidenbecher T, Sosulina L, Lesting J, Sangha S et al. Neuropeptide S-mediated control of fear expression and extinction: role of intercalated GABAergic neurons in the amygdala. Neuron 2008; 59 (2): 298-310. doi: 10.1016/j. neuron.2008.07.002
  • 43. Martig AK, Mizumori SJ. Ventral tegmental area disruption selectively affects CA1/CA2 but not CA3 place fields during a differential reward working memory task. Hippocampus 2011; 21 (2): 172-184. doi: 10.1002/hipo.20734
  • 44. Solari N, Bonito-Oliva A, Fisone G, Brambilla R. Understanding cognitive deficits in Parkinson’s disease: lessons from preclinical animal models. Learning Memory 2013; 20 (10): 592-600. doi: 10.1101/lm.032029.113
  • 45. Ferro MM, Bellissimo MI, Anselmo-Franci JA, Angellucci ME, Canteras NS et al. Comparison of bilaterally 6-OHDA- and MPTP-lesioned rats as models of the early phase of Parkinson’s disease: histological, neurochemical, motor and memory alterations. Journal of Neuroscience Methods 2005; 148 (1): 78-87. doi: 10.1016/j.jneumeth.2005.04.005
  • 46. Kim KS, Zhao TT, Shin KS, Park HJ, Cho YJ et al. Gynostemma pentaphyllum ethanolic extract protects against memory deficits in an MPTP-lesioned mouse model of Parkinson’s disease treated with L-DOPA. Journal of Medicinal Food 2017; 20 (1): 11-18. doi: 10.1089/jmf.2016.3764
  • 47. Sy HN, Wu SL, Wang WF, Chen CH, Huang YT et al. MPTPinduced dopaminergic degeneration and deficits in object recognition in rats are accompanied by neuroinflammation in the hippocampus. Pharmacology, Biochemistry, and Behavior 2010; 95 (2): 158-165. doi: 10.1016/j.pbb.2009.12.020
  • 48. Moriguchi S, Yabuki Y, Fukunaga K. Reduced calcium/ calmodulin-dependent protein kinase II activity in the hippocampus is associated with impaired cognitive function in MPTP-treated mice. Journal of Neurochemistry 2012; 120 (4): 541-551. doi: 10.1111/j.1471-4159.2011.07608.x
  • 49. Parsons RL, Ellinwood N, Zylstra T, Greiner A, Johnson B et al. Use of a radial arm maze to assess cognition in normal and MPS IIIB affected dogs. Molecular Genetics and Metabolism 2016; 117 (2): S90-S91. doi: 10.1016/j.ymgme.2015.12.392
  • 50. Prediger RD, Aguiar AS, Jr., Rojas-Mayorquin AE, Figueiredo CP, Matheus FC et al. Single intranasal administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in C57BL/6 mice models early preclinical phase of Parkinson’s disease. Neurotoxicity Research 2010; 17 (2): 114-129. doi: 10.1007/ s12640-009-9087-0
  • 51. Prediger RD, Batista LC, Medeiros R, Pandolfo P, Florio JC et al. The risk is in the air: Intranasal administration of MPTP to rats reproducing clinical features of Parkinson’s disease. Experimental Neurol 2006; 202 (2): 391-403. doi: 10.1016/j. expneurol.2006.07.001
  • 52. Chiaravalloti ND, Ibarretxe-Bilbao N, DeLuca J, Rusu O, Pena J et al. The source of the memory impairment in Parkinson’s disease: acquisition versus retrieval. Movement Disorders 2014; 29 (6): 765-771. doi: 10.1002/mds.25842
  • 53. Lemon N, Manahan-Vaughan D. Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. The Journal of Neuroscience 2006; 26 (29): 7723-7729. doi: 10.1523/ JNEUROSCI.1454-06.2006
  • 54. Costa C, Sgobio C, Siliquini S, Tozzi A, Tantucci M et al. Mechanisms underlying the impairment of hippocampal longterm potentiation and memory in experimental Parkinson’s disease. Brain 2012; 135 (Pt 6): 1884-1899. doi: 10.1093/brain/ aws101
  • 55. Gruszka A, Bor, D., Barker, R., Necka, E., Owen, A. The role of executive processes in working memory deficits in Parkinson’s disease. Polish Psychological Bulletin 2016; 47 (1): 123-130. doi: 10.1515/ppb-2016-0013
  • 56. Barone P. Neurotransmission in Parkinson’s disease: beyond dopamine. European Journal of Neurology 2010; 17 (3): 364- 376. doi: 10.1111/j.1468-1331.2009.02900.x
  • 57. Silva TP, Poli A, Hara DB, Takahashi RN. Time course study of microglial and behavioral alterations induced by 6-hydroxydopamine in rats. Neuroscience Letters 2016; 622: 83-87. doi: 10.1016/j.neulet.2016.04.049
  • 58. Santiago RM, Barbieiro J, Lima MM, Dombrowski PA, Andreatini R et al. 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. Progress in Neuropsychopharmacology and Biological Psychiatry 2010; 34 (6): 1104-1114. doi: 10.1016/j.pnpbp.2010.06.004
  • 59. Schrag A. Psychiatric aspects of Parkinson’s disease--an update. Journal of Neurology 2004; 251 (7): 795-804. doi: 10.1007/ s00415-004-0483-3
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