629
Views
7
CrossRef citations to date
0
Altmetric
Original Paper

Agmatine, A Metabolite of Arginine, Improves Learning and Memory in Streptozotocin-Induced Alzheimer's Disease Model in Rats

, , &
Pages 342-354 | Received 15 Nov 2016, Accepted 31 Dec 2016, Published online: 25 Jan 2017

References

  • Sonkusare SK, Kaul CL, Ramarao P. Dementia of Alzheimer's disease and other neurodegenerative disorders-memantine, a new hope. Pharmacol Res 2005; 51(1): 1–17. [CrossRef]
  • Newman M, Musgrave IF, Lardelli M. Alzheimer disease: amyloidogenesis, the presenilins and animal models. Biochim Biophys Acta 2007; 1772(3): 285–97. [CrossRef]
  • Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 2007; 8(2): 101–12. [CrossRef]
  • Chong ZZ, Li F, Maiese K. Stress in the brain: novel cellular mechanisms of injury linked to Alzheimer's disease. Brain Res Brain Res Rev 2005; 49(1): 1–21. [CrossRef]
  • Pratico D. Oxidative stress hypothesis in Alzheimer's disease: a reappraisal. Trends Pharmacol Sci 2008; 29(12): 609–15. [CrossRef]
  • Salminen A, Ojala J, Kauppinen A, Kaarniranta K, Suuronen T. Inflammation in Alzheimer's disease: amyloid-beta oligomers trigger innate immunity defence via pattern recognition receptors. Prog Neurobiol 2009; 87(3): 181–94. [CrossRef]
  • Hynd MR, Scott HL, Dodd PR. Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem Int 2004; 45(5): 583–95. [CrossRef]
  • Auguet M, Viossat I, Marin JG, Chabrier PE. Selective inhibition of inducible nitric oxide synthase by agmatine. Jpn J Pharmacol 1995; 69(3): 285–7. [CrossRef]
  • Mun CH, Lee WT, Park KA, Lee JE. Regulation of endothelial nitric oxide synthase by agmatine after transient global cerebral ischemia in rat brain. Anat Cell Biol 2010; 43(3): 230–40. [CrossRef]
  • Aricioglu F, Kan B, Yillar O, Korcegez E, Berkman K. Effect of agmatine on electrically and chemically induced seizures in mice. Ann N Y Acad Sci 2003; 1009: 141–6. [CrossRef]
  • Luszczki JJ, Czernecki R, Wojtal K, Borowicz KK, Czuczwar SJ. Agmatine enhances the anticonvulsant action of phenobarbital and valproate in the mouse maximal electroshock seizure model. J Neural Transm (Vienna) 2008; 115(11): 1485–94. [CrossRef]
  • Gilad GM, Salame K, Rabey JM, Gilad VH. Agmatine treatment is neuroprotective in rodent brain injury models. Life Sci 1996; 58(2): 41–6.
  • Gilad GM, Gilad VH. Acclerated functional recovery and neuroprotection by agmatine after spinal cord ischemia. Neurosci Lett 2000; 296(2–3): 97–100. [CrossRef]
  • Wang WP, Iyo AH, Miguel-Hidalgo J, Regunathan S, Zhu MY. Agmatine protects against cell damage induced by NMDA and glutamate in cultured hippocampal neurons. Brain Res 2006; 1084(1): 210–6. [CrossRef]
  • Kim JH, Yenari MA, Giffard RG, Cho SW, Park KA, Lee JE. Agmatine reduces infarct area in a mouse model of transient focal cerebral ischemia and protects cultured neurons from ischemia-like injury. Exp Neurol 2004; 189(1): 122–30. [CrossRef]
  • Aricioglu F, Altunbas H. Is agmatine an endogenous anxiolytic/antidepressant agent. Ann N Y Acad Sci 2003; 1009: 136–40. [CrossRef]
  • Aricioglu F, Regunathan S. Agmatine attenuates stress- and lipopolysaccharide-induced fever in rats. Physiol Behav 2005; 85(3): 370–5. [CrossRef]
  • Aricioglu F, Regunathan S, Piletz JE. Is agmatine an endogenous factor against stress? Ann NY Acad Sci 2003; 1009: 127–32. [CrossRef]
  • Aricioglu-Kartal F, Uzbay IT. Inhibitory effect of agmatine on naloxone precipitated abstinence syndrome in morphine dependent rats. Life Sci 1997; 61(18): 1775–81. [CrossRef]
  • Aricioglu-Kartal F, Regunathan S. Effect of chronic morphine treatment on the biosynthesis of agmatine in rat brain and other tissues. Life Sci 2002; 71(14): 1695–701. [CrossRef]
  • Aricioglu F, Means A, Regunathan S. Effect of agmatine on the development of morphine dependence in rats: potential role of cAMP system. Eur J Pharmacol 2004; 540(3): 191–97. [CrossRef]
  • Aricioglu F, Paul IA, Regunathan S. Agmatine reduces only peripheral-related behavioral signs, not the central signs, of morphine withdrawal in nNOS deficient transgenic mice. Neurosci Lett 2004; 354(2): 153–7. [CrossRef]
  • Santos AR, Gadotti VM, Oliveira GL, Tibola D, Paszcuk AF, Neto A, et al. Mechanisms involved in the antinociception caused by agmatine in mice. Neuropharmacology 2005; 48(7): 1021–34. [CrossRef]
  • Regunathan S, Feinstein DL, Reis DJ. Anti-proliferative and anti-inflammatory actions of imidazoline agents. Are imidazoline receptors involved? Ann N Y Sci 1999; 881: 410–9. [CrossRef]
  • Aricioglu F, Korcegez E, Bozkurt A, Ozyalcin S. Effect of agmatine on acute and mononeuropathic pain. Ann N Y Acad Sci 2003; 1009: 106–15. [CrossRef]
  • Liu P, Collie ND, Chary S, Jing Y, Zhang H. Spatial learning results in elevated agmatine levels in the rat brain. Hippocampus 2008; 18(11): 1094–8. [CrossRef]
  • 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): 951–61. [CrossRef]
  • Liu P, Chary S, Devaraj R, Jing Y, Darlington CL, Smith PF, et al. Effects of aging on agmatine levels in memory-associated brain structures. Hippocampus 2008; 18(9): 853–6. [CrossRef]
  • Qiu WW, Zheng RY. Neuroprotective effects of receptor imidazoline 2 and its endogenous ligand agmatine. Neurosci Bull 2006; 22(3): 187–91.
  • Gumru S, Sahin C, Aricioglu F. Role of agmatine in cognitive functions. OA Behavioural Medicine 2013; 1(1): 1–8.
  • Galea E, Regunathan S, Eliopoulus V, Feinstein DL, Reis DJ. Inhibition of mammalian nitric oxide synthases by agmatine, an endogenous polyamine formed by decarboxylation of arginine. Biochem J 1996; 316(Pt 1): 247–9. [CrossRef]
  • Sharma M, Gupta YK. Intracerebroventricular injection of streptozotocin in rats produces both oxidative stress in the brain and cognitive impairment. Life Sci 2001; 68: 1021–129. [CrossRef]
  • Paxinos G, Watson C. (1998). The rat brain in stereotaxic coordinates. 4nd ed, Academic Press, California.
  • Venable N, Kelly PH. Effects of NMDA receptor antagonists on passive avoidance learning and retrieval in rats and mice. Psychopharmacology (Berl) 1990; 100(2): 215–21. [CrossRef]
  • Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 2001; 11(1): 47–60. [CrossRef]
  • Beutler E. Glutathione in red blood cell metabolism. In: Beutler E, ed. A manual of biochemical methods. New York: Grune and Stratton; 1975. p. 112–4.
  • Beuge JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978; 52: 302–10. [CrossRef]
  • Hillegass LM, Geriswold DE, Brickson B, Albrightson-Winslow C. Assessment of myeloperoxidase activity in whole rat kidney. J Pharmacol Methods 1990; 24(4): 285–95. [CrossRef]
  • Lannert H, Hoyer S. Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav Neurosci 1998; 112(5): 1199–208. [CrossRef]
  • Charles V, Mufson EJ, Friden PM, Bartus RT, Kordower JH. Atrophy of cholinergic basal forebrain neurons following excitotoxic cortical lesions is reversed by intravenous administration of an NGF conjugate. Brain Res 1996; 728(2): 193–203. [CrossRef]
  • Utkan T, Gocmez SS, Regunathan S, Aricioglu F. Agmatine, a metabolite of L-arginine, reverses scopolamine-induced learning and memory impairment in rats. Pharmacol Biochem Behav 2012; 102(4): 578–84. [CrossRef]
  • Moosavi M, Zarifkar AH, Farbood Y, Dianat M, Sarkaki A, Ghasemi R. Agmatine protects against intracerebroventricular streptozotocin-induced water maze memory deficit, hippocampal apoptosis and Akt/GSK3β signaling disruption. Eur J Pharmacol 2014; 736: 107–14. [CrossRef]
  • Rushaidhi M, Zhang H, Liu P. Effects of prolonged agmatine treatment in aged male Sprague-Dawley rats. Neuroscience 2013; 234: 116–24. [CrossRef]
  • Rushaidhi M, Collie ND, Zhang H, Liu P. Agmatine selectively improves behavioural function in aged male Sprague-Dawley rats. Neuroscience 2012; 218: 206–15. [CrossRef]
  • Bergin DH, Jing Y, Zhang H, Liu P. A single intracerebroventricular Aβ25-35 infusion leads to prolonged alterations in arginine metabolism in the rat hippocampus and prefrontal cortex. Neuroscience 2015; 298: 367–79. [CrossRef]
  • Bhutada P, Mundhada Y, Humane V, Rahigude A, Deshmukh P, Latad S, 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. [CrossRef]
  • Rushaidhi M, Jing Y, Kennard JT, Collie ND, Williams JM, Zhang H, et al. Aging affects L-arginine and its metabolites in memory-associated brain structures at the tissue and synaptoneurosome levels. Neuroscience 2012; 209: 21–31. [CrossRef]
  • Zhu MY, Piletz JE, Halaris A, Regunathan S. Effect of agmatine against cell death induced by NMDA and glutamate in neurons and PC12 cells. Cell Mol Neurobiol 2003; 23(4–5): 865–72. [CrossRef]
  • Zarifkar A, Choopani S, Ghasemi R, Naghdi N, Maghsoudi AH, Maghsoudi N, et al. Agmatine prevents LPS-induced spatial memory impairment and hippocampal apoptosis. Eur J Pharmacol 2010; 634(1–3): 84–8. [CrossRef]
  • Sugiura T, Tsutsui H, Takaoka M, Kobuchi S, Hayashi K, Fujii T, et al. Protective effect of agmatine on ischemia/reperfusion-induced renal injury in rats. J Cardiovasc Pharmacol 2008; 51(3): 223–30. [CrossRef]
  • Lee WT, Hong S, Yoon SH, Kim JH, Park KA, Seong GJ, et al. Neuroprotective effects of agmatine on oxygen-glucose deprived primary-cultured astrocytes and nuclear translocation of nuclear factor-kappa B. Brain Res 2009; 1281: 64–70. [CrossRef]
  • Sugiura T, Kobuchi S, Tsutsui H, Takaoka M, Fujii T, Hayashi K, et al. Preventive mechanisms of agmatine against ischemic acute kidney injury in rats. Eur J Pharmacol 2009; 603(1–3): 108–13. [CrossRef]
  • Zhu MY, Wang WP, Huang J, Feng YZ, Regunathan S, Bissette G. Repeated immobilization stress alters rat hippocampal and prefrontal cortical morphology in parallel with endogenous agmatine and arginine decarboxylase levels. Neurochem Int 2008; 53(6–8): 346–54. [CrossRef]
  • Cunha AS, Matheus FC, Moretti M, Sampaio TB, Poli A, Santos DB, et al. Agmatine attenuates reserpine-induced oral dyskinesia in mice: Role of oxidative stress, nitric oxide and glutamate NMDA receptors. Behav Brain Res 2016; 312: 64–76. [CrossRef]
  • Arndt MA, Battaglia V, Parisi E, Lortie MJ, Isome M, Baskerville C, et al. The arginine metabolite agmatine protects mitochondrial function and confers resistance to cellular apoptosis. Am J Physiol Cell Physiol 2009; 296(6): C1411–9. [CrossRef]
  • Demady DR, Jianmongkol S, Vuletich JL, Bender AT, Osawa Y. Agmatine enhances the NADPH oxidase activity of neuronal NO synthase and leads to oxidative inactivation of the enzyme. Mol Pharmacol 2001; 59(1): 24–9.
  • Sirvanci-Yalabik M, Sehirli O, Utkan T, Aricioglu F. Effects of agmatine in streptozotocine induced experimental alzheimer model. Journal of Marmara University Institute of Health Sciences 2013; 3(3): 145–53. (Turkish)
  • Zhu MY, Wang WP, Huang J, Regunathan S. Chronic treatment with glucocorticoids alters rat hippocampal and prefrontal cortical morphology in parallel with endogenous agmatine and arginine decarboxylase levels. J Neurochem 2007; 103(5): 1811–20. [CrossRef]

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.