Role of the cholinergic muscarinic receptors of the CA1 area in the memory impairment induced by iron oxide nanoparticle in adult male rats

Document Type : Research Paper

Authors

Department of Biology, Faculty of Sciences, Shahid Chamran University of Ahvaz, Ahvaz, Iran

Abstract

Objective(s): Nanoparticles of iron oxide (nFe2O3) are widely used in medicine and industry and could interfere with the brain processes associated with memory. The involvement of muscarinic cholinergic receptors in the process of memory formation has been confirmed. The present study aimed to investigate the possible interference of the cholinergic muscarinic receptors of the dorsal hippocampal CA1 area in the memory impairment induced by nFe2O3 in adult male rats.
Materials and Methods: In this study, we examined the possible involvement of the cholinergic muscarinic receptors of the dorsal hippocampal CA1 area in the memory impairment induced by nFe2O3. In total, 70 male rats were divided into 10 groups of saline (1 µl/rat)+saline (1 ml/kg; intraperitoneal [IP]), saline (1 µl/rat)+nFe2O3 (5 and 7.5 mg/kg; IP), pilocarpine (1 and 2 µg/rat)+saline (1 ml/kg), pilocarpine (1 and 2 µg/rat)+nFe2O3 (7.5 mg/kg; IP), scopolamine (1 and 2 µg/rat)+saline (1 ml/kg), and scopolamine (1 µg/rat)+ nFe2O3 (5 mg/kg; IP).
Results: Pilocarpine and scopolamine were injected intra-CA1 after training and before the IP administration of nFe2O3. The latency to enter the dark compartment in the step-through apparatus and locomotor activity was performed on the animals in an open field at 24 hours and seven days after training. The results indicated that nFe2O3 (7.5 mg/kg) decreased memory retrieval (P

Keywords


1. Kandel ER, Dudai Y, Mayford MR. The molecular and systems biology of memory. Cell. 2014; 157(1): 163-186.
2. Abel T, Lattal KM. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol. 2001; 11(2): 180-187.
3. Savic MM, Obradovic DI, Ugrešic ND, Bokonjic DR. Memory effects of benzodiazepines: memory stages and types versus binding-site subtypes. Neural Plast. 2005; 12(4): 289-298.
4. Wang B, Chen YC, Jiang G, Ning Q, Ma L, Chan WY, Wu S, Zhou GQ, Bao R, Zheng ZC, Yang X. New learning and memory related pathways among the hippocampus, the amygdala and the ventromedial region of the striatum in rats. J Chem Neuroanat. 2016; 1; 71: 13-19.
5. Yan BC, Jeon YH, Park JH, Kim IH, Cho JH, Ahn JH, Chen BH, Tae HJ, Lee JC, Ahn JY, Kim DW. Increased cyclooxygenase-2 and nuclear factor-κB/p65 expression in mouse hippocampi after systemic administration of tetanus toxin. Mol Med Rep. 2015; 12(6): 7837-7844.
6. Knowles WD. Normal anatomy and neurophysiology of the hippocampal formation. J Clinl Neurophysiol. 1992; 9(2): 253-263.
7 Khakpai F, Nasehi M, Haeri-Rohani A, Eidi A, Zarrindast MR. Septo-hippocampo-septal loop and memory formation. Basic Clin Neurosci. 2013; 4(1): 5-23.
8. Tiwari P, Dwivedi S, Singh MP, Mishra R, Chandy A. Basic and modern concepts on cholinergic receptor: A review. Asian Pac J Trop Dis. 2013; 3(5): 413-420.
9. Blake MG, Krawczyk MD, Baratti CM, Boccia MM. Neuropharmacology of memory consolidation and reconsolidation: Insights on central cholinergic mechanisms. J Physiol-Paris. 2014; 108(4-6): 286-291.
10. Yakel JL. Cholinergic receptors: functional role of nicotinic ACh receptors in brain circuits and disease. Pflügers Arch. 2013; 465(4): 441-450.
11 Maurer SV, Williams CL. The cholinergic system modulates memory and hippocampal plasticity via its interactions with non-neuronal cells. Front Immunol. 2017; 8: 1489.
12. Dennis SH, Pasqui F, Colvin EM, Sanger H, Mogg AJ, Felder CC, Broad LM, Fitzjohn SM, Isaac JT, Mellor JR. Activation of muscarinic M1 acetylcholine receptors induces long-term potentiation in the hippocampus. Cereb Cortex. 2015; 15; 26(1): 414-426.
13. Sarlak Z, Oryan S, Moghaddasi M. Interaction between the antioxidant activity of curcumin and cholinergic system on memory retention in adult male Wistar rats. Iran Jl Basic Med Sci. 2015; 18(4): 398-403.
14. Thomas M, Jankovic J. Neurodegenerative disease and iron storage in the brain. Curr Opin Neurol. 2004; 17(4): 437-442.
15. Salvador GA. Iron in neuronal function and dysfunction. BioFactors. 2010; 1; 36(2): 103-110.
16. Uranga RM, Salvador GA. Unraveling the burden of iron in neurodegeneration: intersections with amyloid beta peptide pathology. Oxid Med Cell Longev. 2018; 2018: 2850341
17. Naqvi S, Samim M, Abdin MZ, Ahmed FJ, Maitra AN, Prashant CK, Dinda AK. Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress. Int J Nanomedicine. 2010; 5:983-989.
18. Dhakshinamoorthy V, Manickam V, Perumal E. Neurobehavioural toxicity of iron oxide nanoparticles in mice. Neurotox Res. 2017; 1; 32(2): 187-203.
19. Wang B, Feng WY, Wang M, Shi JW, Zhang F, Ouyang H, Zhao YL, Chai ZF, Huang YY, Xie YN, Wang HF. Transport of intranasally instilled fine Fe2O3 particles into the brain: micro-distribution, chemical states, and histopathological observation. Biol Trace Elem res. 2007; 118(3): 233-243.
20. Zarrindast MR, Ardjmand A, Ahmadi S, Rezayof A. Activation of dopamine D1 receptors in the medial septum improves scopolamine-induced amnesia in the dorsal hippocampus. Behav Brain Res. 2012; 229(1): 68-73.
21. Bemani LS. The interaction ofcholinergic muscarinin and beta-1 adrenergic recepors of the CA1 region in passive avoidance memory formation n rat .J Babol Univ Med
22. Khorshidi M, Kesmati M, Khajeh Pour L, Najaf Zadeh Varzi H. Comparison of the effect of iron oxide nanoparticles and bulk on the memory and associated alterations in dopamine and serotonin levels in the hippocampus of adult male rats. Physiol Pharmacol. 2013; 17(2): 204-215.
23. Torabi M, Kesmati M, Harooni HE, Varzi HN. Effect of intra CA1 and intraperitoneal administration of opioid receptor modulating agents on the anxiolytic properties of nano and conventional ZnO in male rats. Cell J (Yakhteh). 2014; 16(2):163-170.
24. Khajehpour L, Rezayof A, Zarrindast MR. Involvement of dorsal hippocampal nicotinic receptors in the effect of morphine on memory retrieval in passive avoidance task. Eur J Pharmacol. 2008; 584(2-3): 343-531.
25. Khakpai F, Nasehi M, Zarrindast MR. The role of NMDA receptors of the medial septum and dorsal hippocampus on memory acquisition. Pharmacol Biochemt Behav. 2016; 143: 18-25.
26. Orta-Salazar E, Cuellar-Lemus CA, Díaz-Cintra S, Feria-Velasco AI. Cholinergic markers in the cortex and hippocampus of some animal species and their correlation to Alzheimer’s disease. Neurología (English Edition). 2014; 29(8): 497-503.
27. Khajehpour L, Fathinia K, Moazedi AA, Kesmati M. Вeta1-Adrenoreceptors of the CA1 Area Mediate Morphine-Modified State-Dependent Memory in Rats. Neurophysiology. 2013; 45(2): 146-152.
28. de Lima MN, Presti-Torres J, Caldana F, Grazziotin MM, Scalco FS, Guimarães MR, Bromberg E, Franke SI, Henriques JA, Schröder N. Desferoxamine reverses neonatal iron-induced recognition memory impairment in rats. Eur J Pharmacol. 2007; 570(1-3): 111-114.
29. Rivet CJ, Yuan Y, Borca-Tasciuc DA, Gilbert RJ. Altering iron oxide nanoparticle surface properties induce cortical neuron cytotoxicity. Chem Res Toxicol. 2011; 25(1): 153-161.
30. Sun Z, Yathindranath V, Worden M, Thliveris JA, Chu S, Parkinson FE, Hegmann T, Miller DW. Characterization of cellular uptake and toxicity of aminosilane-coated iron oxide nanoparticles with different charges in central nervous system-relevant cell culture models. Int J Nanomedicine. 2013; 961-970.
31. Wu J, Ding T, Sun J. Neurotoxic potential of iron oxide nanoparticles in the rat brain striatum and hippocampus. Neurotoxicology. 2013; 34: 243-53.
32. Roesler R, Schröder N. Cognitive enhancers: focus on modulatory signaling influencing memory consolidation. Pharmacol Biochem Behav. 2011; 99(2): 155-163.
33. Knox D. The role of basal forebrain cholinergic neurons in fear and extinction memory. Neurobiology of Learning and Memory. 2016; 133: 39-52.
34. Blokland A, Honig W, Raaijmakers WG. Effects of intra-hippocampal scopolamine injections in a repeated spatial acquisition task in the rat. Psychopharmacology. 1992; 109(3): 373-376.
35. Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, Rahnama NP, Nathanson NM, Silva AJ. Selective cognitive dysfunction in acetylcholine M 1 muscarinic receptor mutant mice. Nat Neuroscie. 2003; 6(1): 51-58.
36. Atri A, Sherman S, Norman KA, Kirchhoff BA, Nicolas MM, Greicius MD, Cramer SC, Breiter HC, Hasselmo ME, Stern CE. Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behav Neurosci. 2004; 118(1): 223-236.
37. Nathan PJ, Watson J, Lund J, Davies CH, Peters G, Dodds CM, Swirski B, Lawrence P, Bentley GD, O’Neill BV, Robertson J. The potent M1 receptor allosteric agonist GSK1034702 improves episodic memory in humans in the nicotine abstinence model of cognitive dysfunction. Int J Neuropsychopharmacol. 2013; 1; 16(4): 721-731.
38. Hasselmo ME. The role of acetylcholine in learning and memory. Curr Opin Neurobiol. 2006; 16(6): 710-715.
39. Bymaster FP, Carter PA, Yamada M, Gomeza J, Wess J, Hamilton SE, Nathanson NM, McKinzie DL, Felder CC. Role of specific muscarinic receptor subtypes in cholinergic parasympathomimetic responses, in vivo phosphoinositide hydrolysis, and pilocarpine‐induced seizure activity. Eur J Neurosci. 2003; 17(7): 1403-1410.
40. Khakpai F, Nasehi M, Haeri-Rohani A, Eidi A, Zarrindast MR. Scopolamine induced memory impairment; possible involvement of NMDA receptor mechanisms of dorsal hippocampus and/or septum. Behav brain res. 2012; 16; 231(1): 1-10.
41. Haider S, Batool Z, Ahmad S, Siddiqui RA, Haleem DJ. Walnut supplementation reverses the scopolamine-induced memory impairment by restoration of cholinergic function via mitigating oxidative stress in rats: a potential therapeutic intervention for age related neurodegenerative disorders.Metab Brain Dis. 2018; 33(1): 39-51.
42. Tota S, Hanif K, Kamat PK, Najmi AK, Nath C. Role of central angiotensin receptors in scopolamine-induced impairment in memory, cerebral blood flow, and cholinergic function. Psychopharmacology. 2012; 222(2): 185-202.
43. Ghasemi S, Moradzadeh M, Hosseini M, Beheshti F, Sadeghnia HR. Beneficial effects of Urtica dioica on scopolamine-induced memory impairment in rats: protection against acetylcholinesterase activity and neuronal oxidative damage. Drug Chem Toxicol. 2019; 42(2): 167-175.
44. Azami NS, Piri M, Oryan S, Jahanshahi M, Babapour V, Zarrindast MR. Involvement of dorsal hippocampal α-adrenergic receptors in the effect of scopolamine on memory retrieval in inhibitory avoidance task. Neurobiol Learn Mem. 2010; 93(4): 455-462.