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Original Articles

Reversal of lipopolysaccharide-induced learning and memory deficits by agmatine in mice

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Pages 621-632 | Received 05 Dec 2019, Accepted 18 Sep 2020, Published online: 18 Jan 2021

References

  • 1. Barker D, Gluckman P, Robinson J. Conference report: fetal origins of adult diseases – report of the first international study group, Sydney. Placenta. 1995;16(3):317–320.
  • 2. Jang H, Boltz D, Sturm-Ramirez K, et al. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci USA. 2009;106(33):14063–14068.
  • 3. Jang H, Boltz D, McClaren J, et al. Inflammatory effects of highly pathogenic H5N1 influenza virus infection in the CNS of mice. J Neurosci. 2012;32(5):1545–1559.,
  • 4. Tenk CM, Kavaliers M, Ossenkopp KP. Neonatal treatment with lipopolysaccharide differentially affects adult anxiety responses in the light-dark test and taste neophobia test in male and female rats. Int J Dev Neurosci. 2013;31(3):171–180.
  • 5. Meehan C, Harms L, Frost JD, et al. Effects of immune activation during early or late gestation on schizophrenia-related behaviour in adult rat offspring. Brain Behav Immun. 2017;63:8–20.
  • 6. Doenni VM, Gray JM, Song CM, et al. Deficient adolescent social behavior following early-life inflammation is ameliorated by augmentation of anandamide signaling. Brain Behav Immun. 2016;58:237–247.
  • 7. Heneka MT, Kummer MP, Latz E. Innate immune activation in neurodegenerative disease. Nat Rev Immunol. 2014;14(7):463–477.
  • 8. Korte M, Schmitz D. Cellular and system biology of memory: timing, molecules, and beyond. Physiol Rev. 2016;96(2):647–693.
  • 9. Lynch MA. Interleukin-1 beta exerts a myriad of effects in the brain and in particular in the hippocampus: analysis of some of these actions. Vitam Horm. 2002;64:185–219.
  • 10. Vitkovic L, Konsman JP, Bockaert J, et al. Cytokine signals propagate through the brain. Mol Psychiatry. 2000;5(6):604–615.
  • 11. Feng Y, Piletz JE, Leblanc MH. Agmatine suppresses nitric oxide production and attenuates hypoxic-ischemic brain injury neonatal rats. Pediatr Res. 2002;52(4):606–611.
  • 12. Gilad GM, Gilad VH, Casanova MF, et al. Polyamines and their metabolizing enzymes in human frontal cortex and hippocampus: preliminary measurements in affective disorders. Biol Psychiatry. 1995;38(4):227–234.
  • 13. Gilad GM, Gilad VH. Accelerated functional recovery and neuroprotection by agmatine after spinal cord ischemia in rats. Neurosci Lett. 2000;296(2–3):97–100.
  • 14. Yu CG, Fairbanks CA, Schreiber KL, et al. Agmatine reverses pain induced by inflammation, neuropathy, and spinal cord injury. Proc Natl Acad Sci USA. 2000;97(19):10584–10589.
  • 15. Moretti M, Matheus FC, de Oliveira PA, et al. Role of agmatine in neurodegenerative diseases and epilepsy. Front Biosci (Elite Ed). 2014;6(6):341–359.
  • 16. Xu W, Gao L, Li T, et al. Neuroprotective role of agmatine in neurological diseases. Curr Neuropharmacol. 2018;16(9):1296–1305.
  • 17. Arteni NS, Lavinsky D, Rodrigues AL, et al. Agmatine facilitates memory of an inhibitory avoidance task in adult rats. Neurobiol Learn Mem. 2002;78(2):465–469.
  • 18. Liu P, Bergin DH. Differential effects of i.c.v. microinfusion of agmatine on spatial working and reference memory in the rat. Neuroscience. 2009;159(3):951–961.
  • 19. McKay BE, Lado WE, Martin LJ, et al. Learning and memory in agmatine-treated rats. Pharmacol Biochem Behav. 2002;72(3):551–557.
  • 20. Moosavi M, Zarifkar AH, Farbood Y, et al. Agmatine protects against intracerebroventricular streptozotocin-induced water maze memory deficit, hippocampal apoptosis and Akt/GSK3β signaling disruption. Eur J Pharmacol. 2014;736:107–114.
  • 21. Rastegar K, Roosta H, Zarifkar A, et al. The effect of intra-CA1 agmatine microinjection on water maze learning and memory in rat. Iran Red Crescent Med J. 2011;13(5):316–322.
  • 22. Zarifkar A, Choopani S, Ghasemi R, et al. Agmatine prevents LPS-induced spatial memory impairment and hippocampal apoptosis. Eur J Pharmacol. 2010;634(1–3):84–88.
  • 23. Bhutada P, Mundhada Y, Humane V, et al. Agmatine, an endogenous ligand of imidazoline receptor protects against memory impairment and biochemical alterations in streptozotocin-induced diabetic rats. Prog Neuropsychopharmacol Biol Psychiatry. 2012;37(1):96–105.
  • 24. Kang HW, Lim WC, Lee JK, et al. Germinated waxy black rice ameliorates hyperglycemia and dyslipidemia in streptozotocin-induced diabetic rats. Biol Pharm Bull. 2017;40(11):1846–1855.
  • 25. Kang S, Kim CH, Jung H, et al. Agmatine ameliorates type 2 diabetes induced-Alzheimer’s disease-like alterations in high-fat diet-fed mice via reactivation of blunted insulin signalling. Neuropharmacology. 2017;113(Pt A):467–479.
  • 26. Gawali NB, Bulani VD, Chowdhury AA, et al. Agmatine ameliorates lipopolysaccharide induced depressive-like behaviour in mice by targeting the underlying inflammatory and oxido-nitrosative mediators. Pharmacol Biochem Behav. 2016;149:1–8.
  • 27. Ahn SK, Hong S, Park YM, et al. Protective effects of agmatine on lipopolysaccharide-injured microglia and inducible nitric oxide synthase activity. Life Sci. 2012;91(25–26):1345–1350.
  • 28. Perry VH. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun. 2004;18(5):407–413.
  • 29. Sell KM, Crowe SF, Kent S. Lipopolysaccharide induces memory-processing deficits in day-old chicks. Pharmacol Biochem Behav. 2001;68(3):497–502.
  • 30. Shaw KN, Commins S, O’Mara SM. Lipopolysaccharide causes deficits in spatial learning in the water maze but notin BDNF expression in the rat dentate gyrus. Behav Brain Res. 2001;124(1):47–54.
  • 31. Sparkman NL, Martin LA, Calvert WS, et al. Effects of intraperitoneal lipopolysaccharide on Morris maze performance in year-old and 2-month-old female C57BL/6J mice. Behav Brain Res. 2005;159(1):145–151.
  • 32. Sheng JG, Bora SH, Xu G, et al. Lipopolysaccharide-induced-neuroinflammation increases intracellular accumulation of amyloid precursor protein and amyloid beta peptide in APPswe transgenic mice. Neurobiol Dis. 2003;14(1):133–145.
  • 33. Hauss-Wegrzyniak B, Dobrzanski P, Stoehr JD, et al. Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer’s disease. Brain Res. 1998;780(2):294–303.
  • 34. Kitazawa M, Oddo S, Yamasaki TR, et al. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci. 2005;25(39):8843–8853.
  • 35. Czerniawski J, Miyashita T, Lewandowski G, et al. Systemic lipopolysaccharide administration impairs retrieval of context-object discrimination, but not spatial, memory: evidence for selective disruption of specific hippocampus-dependent memory functions during acute neuroinflammation. Brain Behav Immun. 2015;44:159–166.
  • 36. Lee JW, Lee YK, Yuk DY, et al. Neuro-inflammation induced by lipopolysaccharide causes cognitive impairment through enhancement of beta-amyloid generation. J. Neuroinflamm. 2008;29:5–37.
  • 37. Nazem A, Sankowski R, Bacher M, et al. Rodent models of neuroinflammation for Alzheimer's disease. J Neuroinflamm. 2015;12:74.
  • 38. Zhu B, Wang ZG, Ding J, et al. Chronic lipopolysaccharide exposure induces cognitive dysfunction without affecting BDNF expression in the rat hippocampus. Exp Ther Med. 2014;7(3):750–754.
  • 39. Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats. Behav Brain Res. 1988;31(1):47–59.
  • 40. Nakhate KT, Bharne AP, Verma VS, et al. Plumbagin ameliorates memory dysfunction in streptozotocin induced Alzheimer's disease via activation of Nrf2/ARE pathway and inhibition of β-secretase. Biomed Pharmacother. 2018;101:379–390.
  • 41. Moosavi M, Khales GY, Abbasi L, et al. Agmatine protects against scopolamine-induced water maze performance impairment and hippocampal ERK and Akt inactivation. Neuropharmacology. 2012;62(5–6):2018–2023.
  • 42. Rong Y, Jiang JX, Hu Y, et al. The immune system drives synapse loss during lipopolysaccharide-induced learning and memory impairment in mice. Front Ageing Neurosci. 2019;11:279.
  • 43. Tellez-Merlo G, Morales-Medina JC, Camacho-Ábrego I, et al. Prenatal immune challenge induces behavioral deficits, neuronal remodeling, and increases brain nitric oxide and zinc levels in the male rat offspring. Neuroscience. 2019;406:594–605.
  • 44. Batista C, Gomes G, Candelario-Jalil E, et al. Lipopolysaccharide-induced neuroinflammation as a bridge to understand neurodegeneration. IJMS. 2019;20(9):2293.
  • 45. Dantzer R, O'Connor JC, Freund GG, et al. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46–56.
  • 46. Ormerod BK, Hanft SJ, Asokan A, et al. PPARγ activation prevents impairments in spatial memory and neurogenesis following transient illness. Brain Behav Immun. 2013;29:28–38.
  • 47. Gu C, Hu Q, Wu J, et al. P7C3 Inhibits LPS-induced microglial activation to protect dopaminergic neurons against inflammatory factor-induced cell death in vitro and in vivo. Front Cell Neurosci. 2018;12:400.
  • 48. Hunter RL, Dragicevic N, Seifert K, et al. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J Neurochem. 2007;100(5):1375–1386.
  • 49. Laye S, Parnet P, Goujon E, et al. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Brain Res Mol Brain Res. 1994;27(1):157–162.
  • 50. Vallieres L, Rivest S. Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1beta. J Neurochem. 1997;69(4):1668–1683.
  • 51. Piletz JE, May PJ, Wang G, et al. Agmatine crosses the blood-brain barrier. Ann N Y Acad Sci. 2003;1009:64–74.

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