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Advances in Medicine
Volume 2016, Article ID 7676512, 8 pages
http://dx.doi.org/10.1155/2016/7676512
Research Article

Lipopolysaccharide-Induced Spatial Memory and Synaptic Plasticity Impairment Is Preventable by Captopril

1Neurocognitive Research Center, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
2Department of Physiology, School of Medicine, Jiroft University of Medical Sciences, Jiroft, Iran
3Department of Physiology, Esfarayen Faculty of Medical Sciences, Esfarayen, Iran
4Neurogenic Inflammation Research Center, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

Received 25 April 2016; Revised 20 August 2016; Accepted 22 September 2016

Academic Editor: João Quevedo

Copyright © 2016 Azam Abareshi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Ciobica, W. Bild, L. Hritcu, and I. Haulica, “Brain renin-angiotensin system in cognitive function: pre-clinical findings and implications for prevention and treatment of dementia,” Acta Neurologica Belgica, vol. 109, no. 3, pp. 171–180, 2009. View at Google Scholar · View at Scopus
  2. J. W. Wright and J. W. Harding, “The brain angiotensin system and extracellular matrix molecules in neural plasticity, learning, and memory,” Progress in Neurobiology, vol. 72, no. 4, pp. 263–293, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. M. J. McKinley, A. L. Albiston, A. M. Allen et al., “The brain renin-angiotensin system: location and physiological roles,” International Journal of Biochemistry and Cell Biology, vol. 35, no. 6, pp. 901–918, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. V. L. Bodiga and S. Bodiga, “Renin angiotensin system in cognitive function and dementia,” Asian Journal of Neuroscience, vol. 2013, Article ID 102602, 18 pages, 2013. View at Publisher · View at Google Scholar
  5. Z. Lenkei, M. Palkovits, P. Corvol, and C. Llorens-Cortès, “Expression of angiotensin type-1 (AT1) and type-2 (AT2) receptor mRNAs in the adult rat brain: a functional neuroanatomical review,” Frontiers in Neuroendocrinology, vol. 18, no. 4, pp. 383–439, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. P. R. Gard, “The role of angiotensin II in cognition and behaviour,” European Journal of Pharmacology, vol. 438, no. 1-2, pp. 1–14, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Llorens-Cortes and F. A. O. Mendelsohn, “Organisation and functional role of the brain angiotensin system,” Journal of the Renin-Angiotensin-Aldosterone System, vol. 3, supplement 1, pp. S39–S48, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Hirawa, Y. Uehara, Y. Kawabata et al., “Long-term inhibition of renin-angiotensin system sustains memory function in aged Dahl rats,” Hypertension, vol. 34, no. 3, pp. 496–502, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. V. Paul and P. Ekambaram, “Involvement of nitric oxide in learning & memory processes,” Indian Journal of Medical Research, vol. 133, no. 5, pp. 471–478, 2011. View at Google Scholar · View at Scopus
  10. A. Anaeigoudari, M. Soukhtanloo, M. N. Shafei et al., “Neuronal nitric oxide synthase has a role in the detrimental effects of lipopolysaccharide on spatial memory and synaptic plasticity in rats,” Pharmacological Reports, vol. 68, no. 2, pp. 243–249, 2016. View at Publisher · View at Google Scholar · View at Scopus
  11. H. Shimizu, M. Miyoshi, K. Matsumoto, O. Goto, T. Imoto, and T. Watanabe, “The effect of central injection of angiotensin-converting enzyme inhibitor and the angiotensin type 1 receptor antagonist on the induction by lipopolysaccharide of fever and brain interleukin-1β response in rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 308, no. 3, pp. 865–873, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Tarkowski, H. Carlsten, H. Herlitz, and G. Westberg, “Differential effects of captopril and enalapril, two angiotensin converting enzyme inhibitors, on immune reactivity in experimental lupus disease,” Agents and Actions, vol. 31, no. 1-2, pp. 96–101, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. A. C. T. M. Peeters, M. G. Netea, B. J. Kullberg, T. Thien, and J. W. M. Van Der Meer, “The effect of renin-angiotensin system inhibitors on pro- and anti- inflammatory cytokine production,” Immunology, vol. 94, no. 3, pp. 376–379, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. K. M. Sell, S. F. Crowe, and S. Kent, “Lipopolysaccharide induces memory-processing deficits in day-old chicks,” Pharmacology Biochemistry and Behavior, vol. 68, no. 3, pp. 497–502, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Tyagi, R. Agrawal, C. Nath, and R. Shukla, “Influence of LPS-induced neuroinflammation on acetylcholinesterase activity in rat brain,” Journal of Neuroimmunology, vol. 205, no. 1-2, pp. 51–56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Anaeigoudari, M. N. Shafei, M. Soukhtanloo et al., “Lipopolysaccharide-induced memory impairment in rats is preventable using 7-nitroindazole,” Arquivos de Neuro-Psiquiatria, vol. 73, no. 9, pp. 784–790, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. H. S. Sharma, “Effect of captopril (a converting enzyme inhibitor) on blood-brain barrier permeability and cerebral blood flow in normotensive rats,” Neuropharmacology, vol. 26, no. 1, pp. 85–92, 1987. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Schindler, C. A. Dinarello, and K.-M. Koch, “Angiotensin-converting-enzyme inhibitors suppress synthesis of tumour necrosis factor and interleukin 1 by human peripheral blood mononuclear cells,” Cytokine, vol. 7, no. 6, pp. 526–533, 1995. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Amirshahrokhi, M. Ghazi-Khansari, A. Mohammadi-Farani, and G. Karimian, “Effect of captopril on TNF-α and IL-10 in the livers of bile duct ligated rats,” Iranian Journal of Immunology, vol. 7, no. 4, pp. 247–251, 2010. View at Google Scholar · View at Scopus
  20. N. Terrando, A. Rei Fidalgo, M. Vizcaychipi et al., “The impact of IL-1 modulation on the development of lipopolysaccharide-induced cognitive dysfunction,” Critical Care, vol. 14, no. 3, article R88, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. C. C. Barney, M. J. Katovich, and M. J. Fregly, “The effect of acute administration of an angiotensin converting enzyme inhibitor, captopril (SQ 14,225), on experimentally induced thirsts in rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 212, no. 1, pp. 53–57, 1980. View at Google Scholar · View at Scopus
  22. D. Kumaran, M. Udayabanu, M. Kumar, R. Aneja, and A. Katyal, “Involvement of angiotensin converting enzyme in cerebral hypoperfusion induced anterograde memory impairment and cholinergic dysfunction in rats,” Neuroscience, vol. 155, no. 3, pp. 626–639, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Łukawski, T. Jakubus, G. Raszewski, and S. J. Czuczwar, “Captopril potentiates the anticonvulsant activity of carbamazepine and lamotrigine in the mouse maximal electroshock seizure model,” Journal of Neural Transmission, vol. 117, no. 10, pp. 1161–1166, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. A. H. Swiergiel and A. J. Dunn, “Effects of interleukin-1β and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests,” Pharmacology Biochemistry and Behavior, vol. 86, no. 4, pp. 651–659, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. N. L. Sparkman, L. A. Martin, W. S. Calvert, and G. W. Boehm, “Effects of intraperitoneal lipopolysaccharide on Morris maze performance in year-old and 2-month-old female C57BL/6J mice,” Behavioural Brain Research, vol. 159, no. 1, pp. 145–151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. T. V. P. Bliss and G. L. Collingridge, “A synaptic model of memory: long-term potentiation in the hippocampus,” Nature, vol. 361, no. 6407, pp. 31–39, 1993. View at Publisher · View at Google Scholar · View at Scopus
  27. A. J. Cunningham, C. A. Murray, L. A. J. O'Neill, M. A. Lynch, and J. J. O'Connor, “Interleukin-1β (IL-1β) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro,” Neuroscience Letters, vol. 203, no. 1, pp. 17–20, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Commins, L. A. J. O'Neill, and S. M. O'Mara, “The effects of the bacterial endotoxin lipopolysaccharide on synaptic transmission and plasticity in the CA1-subiculum pathway in vivo,” Neuroscience, vol. 102, no. 2, pp. 273–280, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. L. M. Thomson and R. J. Sutherland, “Systemic administration of lipopolysaccharide and interleukin-1β have different effects on memory consolidation,” Brain Research Bulletin, vol. 67, no. 1-2, pp. 24–29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. W. P. Luk, Y. Zhang, T. D. White et al., “Adenosine: a mediator of interleukin-1β-induced hippocampal synaptic inhibition,” Journal of Neuroscience, vol. 19, no. 11, pp. 4238–4244, 1999. View at Google Scholar · View at Scopus
  31. A. Anaeigoudari, M. Soukhtanloo, P. Reisi, F. Beheshti, and M. Hosseini, “Inducible nitric oxide inhibitor aminoguanidine, ameliorates deleterious effects of lipopolysaccharide on memory and long term potentiation in rat,” Life Sciences, vol. 158, pp. 22–30, 2016. View at Publisher · View at Google Scholar
  32. O. von Bohlen und Halbach and D. Albrecht, “The CNS renin-angiotensin system,” Cell and Tissue Research, vol. 326, no. 2, pp. 599–616, 2006. View at Publisher · View at Google Scholar
  33. I. Haulică, W. Bild, and D. Boişteanu, “Biosynthesis and physio-pharmacological actions of angiotensin peptides: 2. Physio-pharmacological properties,” Revista Medico-Chiruricala A Societatii de Medici si Naturalisti Din Iasi, vol. 110, no. 2, pp. 384–390, 2006. View at Google Scholar · View at Scopus
  34. S. Inaba, M. Iwai, M. Furuno et al., “Continuous activation of renin-angiotensin system impairs cognitive function in renin/angiotensinogen transgenic mice,” Hypertension, vol. 53, no. 2, pp. 356–362, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. W. Bild, L. Hritcu, A. Ciobica, V. Artenie, and I. Haulica, “P02-170 Comparative effects of captopril, losartan and PD123319 on the memory processes in rats,” European Psychiatry, vol. 24, p. S860, 2009. View at Publisher · View at Google Scholar
  36. H. Sepehri, F. Ganji, and F. Bakhshandeh, “Effect of short time captopril administration on spatial memory in aging rats,” Physiology and Pharmacology, vol. 19, no. 1, pp. 68–75, 2015. View at Google Scholar · View at Scopus
  37. M. H. Skinner, D.-X. Tan, M. Grossmann, M. T. Pyne, and R. K. Mahurin, “Effects of captopril and propranolol on cognitive function and cerebral blood flow in aged hypertensive rats,” Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, vol. 51, no. 6, pp. B454–B460, 1996. View at Google Scholar · View at Scopus
  38. O. Marson, A. B. Ribeiro, S. Tufik, O. Kohlmann Jr., and O. L. Ramos, “Inhibition of central angiotensin I conversion by oral captopril,” Brazilian Journal of Medical and Biological Research, vol. 14, no. 1, pp. 73–76, 1981. View at Google Scholar · View at Scopus
  39. S. Kato, K. Itoh, T. Yaoi et al., “Organ distribution of quantum dots after intraperitoneal administration, with special reference to area-specific distribution in the brain,” Nanotechnology, vol. 21, no. 33, Article ID 335103, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. A. R. Brasier, A. Recinos, and M. S. Eledrisi, “Vascular inflammation and the renin-angiotensin system,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 22, no. 8, pp. 1257–1266, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. R. J. Bolterman, M. C. Manriquez, M. C. Ortiz Ruiz, L. A. Juncos, and J. C. Romero, “Effects of captopril on the renin angiotensin system, oxidative stress, and endothelin in normal and hypertensive rats,” Hypertension, vol. 46, no. 4, pp. 943–947, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Amirshahrokhi, M. Ghazi-Khansari, A. Mohammadi-Farani, and G. Karimian, “Effect of captopril on TNF-α and IL-10 in the livers of bile duct ligated rats,” Iranian Journal of Immunology, vol. 7, no. 4, pp. 247–251, 2010. View at Google Scholar · View at Scopus
  43. A. Zagariya, R. Bhat, S. Navale, G. Chari, and D. Vidyasagar, “Inhibition of meconium-induced cytokine expression and cell apoptosis by pretreatment with captopril,” Pediatrics, vol. 117, no. 5, pp. 1722–1727, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Beheshti, M. Hosseini, M. N. Shafei et al., “The effects of Nigella sativa extract on hypothyroidism-associated learning and memory impairment during neonatal and juvenile growth in rats,” Nutritional Neuroscience, 2016. View at Publisher · View at Google Scholar
  45. K. Husain, W. Hernandez, R. A. Ansari, and L. Ferder, “Inflammation, oxidative stress and renin angiotensin system in atherosclerosis,” World Journal of Biological Chemistry, vol. 6, no. 3, pp. 209–217, 2015. View at Publisher · View at Google Scholar
  46. M. Pacurari, R. Kafoury, P. B. Tchounwou, and K. Ndebele, “The renin-angiotensin-aldosterone system in vascular inflammation and remodeling,” International Journal of Inflammation, vol. 2014, Article ID 689360, 13 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. N.-C. Li, A. Lee, R. A. Whitmer et al., “Use of angiotensin receptor blockers and risk of dementia in a predominantly male population: prospective cohort analysis,” British Medical Journal, vol. 340, Article ID b5465, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. E. M. V. de Cavanagh, F. Inserra, L. Ferder, and C. G. Fraga, “Enalapril and captopril enhance glutathione-dependent antioxidant defenses in mouse tissues,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 278, no. 3, pp. R572–R577, 2000. View at Google Scholar · View at Scopus
  49. A. Abareshi, M. Hosseini, M. N. Shafei, M. H. Boskabady, and H. R. Sadeghnia, The effects of captopril on behavioral dysfunctions induced by lipopolysaccharide in male rats [M.S. of Physiology], School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran, 2016.
  50. M. Tamba and A. Torreggiani, “Free radical scavenging and copper chelation: a potentially beneficial action of captopril,” Free Radical Research, vol. 32, no. 3, pp. 199–211, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Niknahad, A. Taghdiri, A. Mohammadi-Bardbori, and A. Rezaeian Mehrabadi, “Protective effect of captopril against doxorubicin-induced oxidative stress in isolated rat liver mitochondria,” Iranian Journal of Pharmaceutical Sciences, vol. 6, no. 2, pp. 91–98, 2010. View at Google Scholar · View at Scopus