Skip to main content
SpringerLink
Log in

Antiamnesic and Antioxidants Effects of Ferulago angulata Essential Oil Against Scopolamine-Induced Memory Impairment in Laboratory Rats

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Ferulago angulata (Apiaceae) is a shrub indigenous to western Iran, Turkey and Iraq. In traditional medicine, F. angulata is recommended for treating digestive pains, hemorrhoids, snake bite, ulcers and as sedative. In the present study, the effects of inhaled F. angulata essential oil (1 and 3 %, daily, for 21 days) on spatial memory performance were assessed in scopolamine-treated rats. Scopolamine-induced memory impairments were observed, as measured by the Y-maze and radial arm-maze tasks. Decreased activities of superoxide dismutase, glutathione peroxidase and catalase along with increase of acetylcholinesterase activity and decrease of total content of reduced glutathione were observed in the rat hippocampal homogenates of scopolamine-treated animals as compared with control. Production of protein carbonyl and malondialdehyde significantly increased in the rat hippocampal homogenates of scopolamine-treated animals as compared with control, as a consequence of impaired antioxidant enzymes activities. Additionally, in scopolamine-treated rats exposure to F. angulata essential oil significantly improved memory formation and decreased oxidative stress, suggesting memory-enhancing and antioxidant effects. Therefore, our results suggest that multiple exposures to F. angulata essential oil ameliorate scopolamine-induced spatial memory impairment by attenuation of the oxidative stress in the rat hippocampus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Xu P-x, Wang S-w, Yu X-l, Su Y-j, Wang T, Zhou W-w, Zhang H, Wang Y-j, Liu R-t (2014) Rutin improves spatial memory in Alzheimer’s disease transgenic mice by reducing Aβ oligomer level and attenuating oxidative stress and neuroinflammation. Behav Brain Res 264:173–180

    Article  Google Scholar 

  2. Mathew M, Subramanian S (2014) In vitro screening for anti-cholinesterase and antioxidant activity of methanolic extracts of ayurvedic medicinal plantsused for cognitive disorders. PLoS ONE 9:e86804

    Article  PubMed Central  PubMed  Google Scholar 

  3. Ebert U, Kirch W (1998) Scopolamine model of dementia: electroencephalogram findings and cognitive performance. Eur J Clin Invest 28:944–949

    Article  CAS  PubMed  Google Scholar 

  4. Klinkenberg I, Blokland A (2010) The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev 34:1307–1350

    Article  CAS  PubMed  Google Scholar 

  5. Eastonn A, Douchamps V, Eacott M, Lever C (2012) A specific role for septohippocampal acetylcholine in memory? Neuropsychologia 50:3156–3168

    Article  Google Scholar 

  6. Kwon SH, Ma SX, Joo HJ, Lee SY, Jang CG (2013) Inhibitory effects of Eucommia ulmoides Oliv. bark on scopolamine-induced learning and memory deficits in mice. Biomol Ther 21:462–469

    Article  Google Scholar 

  7. Moreira PI, Nunomura A, Nakamura M, Takeda A, Shenk JC, Aliev G, Smith MA, Perry G (2008) Nucleic acid oxidation in Alzheimer disease. Free Radic Biol Med 44:1493–1505

    Article  CAS  PubMed  Google Scholar 

  8. Ischiropoulos H, Beckman JS (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest 111:163–169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Luque-Contreras D, Carvajal K, Toral-Rios D, Franco-Bocanegra D, Campos-Pena V (2014) Oxidative stress and metabolic syndrome: cause or consequence of Alzheimer’s disease? Oxid Med Cell Longev 2014. Article ID 497802:11

    Google Scholar 

  10. Dumont M, Beal MF (2011) Neuroprotective strategies involving ROS in Alzheimer disease. Free Radic Biol Med 51:1014–1026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Coppede F, Migliore L (2009) DNA damage and repair in Alzheimer’s disease. Curr Alzheimer Res 6:36–47

    Article  CAS  PubMed  Google Scholar 

  12. Lovell MA, Markesbery WR (2008) Oxidatively modified RNA in mild cognitive impairment. Neurobiol Dis 29:169–175

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Pinto E, Hrimpeng K, Lopes G, Vaz S, Gonçalves MJ, Cavaleiro C, Salgueiro L (2013) Antifungal activity of Ferulago capillaris essential oil against Candida, Cryptococcus, Aspergillus and dermatophyte species. Eur J Clin Microbiol Infect Dis 32:1311–1320

    Article  CAS  PubMed  Google Scholar 

  14. Pirbalouti A, Sedaghat L, Hamedi B, Tirgir F (2013) Chemical composition and antioxidant activity of essential oils of three endemic medicinal plants of Iran. Bangl J Bot 42:327–332

    Google Scholar 

  15. Rafieian-kopaei M, Shahinfard N, Rouhi-Boroujeni H, Gharipour M, Darvishzadeh-Boroujeni P (2014) Effects of Ferulago angulata extract on serum lipids and lipid peroxidation. Evid Based Complement Alternat Med 2014, Article ID 680856:4

  16. Adams RP (2007) Identification of essential oil by Gas Chromatography/Mass Spectroscopy. Allured Publishing Corporation, Carol Stream, Illinois

    Google Scholar 

  17. Gradinariu V, Cioanca O, Hritcu L, Trifan A, Gille E, Hancianu M (2014) Comparative efficacy of Ocimum sanctum L. and Ocimum basilicum L. essential oils against amyloid beta (1–42)-induced anxiety and depression in laboratory rats. Phytochem Rev. doi:10.1007/s11101-014-9389-6

  18. Linck VM, da Silva AL, Figueiró M, Caramão EB, Moreno PRH, Elisabetsky E (2010) Effects of inhaled Linalool in anxiety, social interaction and aggressive behavior in mice. Phytomedicine 17:679–683

    Article  CAS  PubMed  Google Scholar 

  19. Hritcu L, Noumedem J, Cioanca O, Hancianu M, Kuete V, Mihasan M (2014) Methanolic extract of Piper nigrum fruits improves memory impairment by decreasing brain oxidative stress in amyloid beta(1–42) rat model of Alzheimer’s disease. Cell Mol Neurobiol 34:437–449

    Article  PubMed  Google Scholar 

  20. Cioanca O, Hritcu L, Mihasan M, Hancianu M (2013) Cognitive-enhancing and antioxidant activities of inhaled coriander volatile oil in amyloid β(1–42) rat model of Alzheimer’s disease. Physiol Behav 120:193–202

    Article  CAS  PubMed  Google Scholar 

  21. Ellman G, Courtney K, Andres VJ, Feather-Stone R (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  PubMed  Google Scholar 

  22. Srikumar B, Ramkumar K, Raju T, Shankaranarayana Rao B (2004) Assay of acetylcholinesterase activity in the brain. In: Raju T, Kutty B, Sathyaprabha T, Shanakranarayana Rao B (eds) Brain and Behavior. National Institute of Mental Health and Neurosciences, Bangalore, pp 142–144

    Google Scholar 

  23. Winterbourn C, Hawkins R, Brian M, Carrell R (1975) The estimation of red cell superoxide dismutase activity. J Lab Clin Med 85:337

    CAS  PubMed  Google Scholar 

  24. Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394

    Article  CAS  PubMed  Google Scholar 

  25. Sharma M, Gupta YK (2002) Chronic treatment with trans resveratrol prevents intracerebroventricular streptozotocin induced cognitive impairment and oxidative stress in rats. Life Sci 7:2489–2498

    Article  Google Scholar 

  26. Fukuzawa K, Tokumura A (1976) Glutathione peroxidase activity in tissues of vitamin E-deficient mice. J Nutr Sci Vitaminol 22:405–407

    Article  CAS  PubMed  Google Scholar 

  27. Oliver CN, Ahn BW, Moerman EJ, Goldstein S, Stadtman ER (1987) Age-related changes in oxidized proteins. J Biol Chem 262:5488–5491

    CAS  PubMed  Google Scholar 

  28. Luo S, Wehr NB (2009) Protein carbonylation: avoiding pitfalls in the 2,4-dinitrophenylhydrazine assay. Redox Rep 14:159–166

    Article  CAS  PubMed  Google Scholar 

  29. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  30. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  31. Chuong NN, Trung BH, Luan TC, Hung TM, Dang NH, Dat NT (2014) Anti-amnesic effect of alkaloid fraction from Lycopodiella cernua (L.) Pic. Serm. on scopolamine-induced memory impairment in mice. Neurosci Lett 575:42–46

    Article  PubMed  Google Scholar 

  32. Lee S, Kim J, Seo SG, Choi B-R, Han J-S, Lee KW, Kim J (2014) Sulforaphane alleviates scopolamine-induced memory impairment in mice. Pharmacol Res 85:23–32

    Article  CAS  PubMed  Google Scholar 

  33. Lee J-S, Kim H-G, Han J-M, Kim D-W, Yi M-H, Son S-W, Kim Y-A, Lee J-S, Choi M-K, Son C-G (2014) Ethanol extract of Astragali Radix and Salviae Miltiorrhizae Radix, Myelophil, exerts anti-amnesic effect in a mouse model of scopolamine-induced memory deficits. J Ethnopharmacol 153:782–792

    Article  CAS  PubMed  Google Scholar 

  34. Park SJ, Jung JM, Lee HE, Lee YW, Kim DH, Kim JM, Hong JG, Lee CH, Jung IH, Cho Y-B, Jang DS, Ryu JH (2012) The memory ameliorating effects of INM-176, an ethanolic extract of Angelica gigas, against scopolamine- or Aβ1–42-induced cognitive dysfunction in mice. J Ethnopharmacol 143:611–620

    Article  CAS  PubMed  Google Scholar 

  35. Kim K, Bu Y, Jeong S, Lim J, Kwon Y, Cha DS, Kim J, Jeon S, Eun J, Jeon H (2006) Memory-enhancing effect of a supercritical carbon dioxide fluid extract of the needles of Abies koreana on scopolamine-induced amnesia in mice. Biosci Biotechnol Biochem 70:1821–1826

    Article  CAS  PubMed  Google Scholar 

  36. Perry NSL, Houghton PJ, Theobald A, Jenner P, Perry EK (2000) In-vitro inhibition of human erythrocyte acetylcholinesterase by Salvia lavandulaefolia essential oil and constituent terpenes. J Pharm Pharmacol 52:895–902

    Article  CAS  PubMed  Google Scholar 

  37. Loizzo MR, Menichini F, Tundis R, Bonesi M, Conforti F, Nadjafi F, Statti GA, Frega NG, Menichini F (2009) In vitro biological activity of Salvia leriifolia benth essential oil relevant to the treatment of Alzheimer’s disease. J Oleo Sci 58:443–446

    Article  CAS  PubMed  Google Scholar 

  38. Falsafi SK, Deli A, Höger H, Pollak A, Lubec G (2012) Scopolamine administration modulates muscarinic, nicotinic and NMDA receptor systems. PLoS ONE 7:e32082

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Tota S, Hanif K, Kamat P, Najmi A, Nath C (2012) Role of central angiotensin receptors in scopolamine-induced impairment in memory, cerebral blood flow, and cholinergic function. Psychopharmacology 222:185–202

    Article  CAS  PubMed  Google Scholar 

  40. Abreu-Villaça Y, Filgueiras CC, Manhães AC (2011) Developmental aspects of the cholinergic system. Behav Brain Res 221:367–378

    Article  PubMed  Google Scholar 

  41. Shi J, Liu Q, Wang Y, Luo G (2010) Coadministration of huperzine A and ligustrazine phosphate effectively reverses scopolamine-induced amnesia in rats. Pharmacol Biochem Behav 96:449–453

    Article  CAS  PubMed  Google Scholar 

  42. Stadtman E (1992) Protein oxidation and aging. Science 257:1220–1224

    Article  CAS  PubMed  Google Scholar 

  43. Lee M-R, Yun B-S, Park S-Y, Ly S-Y, Kim S-N, Han B-H, Sung C-K (2010) Anti-amnesic effect of Chong–Myung–Tang on scopolamine-induced memory impairments in mice. J Ethnopharmacol 132:70–74

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Emel Aydin was supported by LLP Erasmus (2013/2014) during her stage within Alexandru Ioan Cuza University of Iasi, Romania.

Author information

Authors and Affiliations

  1. Department of Biology, Alexandru Ioan Cuza University of Iasi, Bd. Carol I, No.11, 700506, Iasi, Romania

    Lucian Hritcu & Marius Mihasan

  2. Department of Biology, Faculty of Science, Firat University, 23119, Elazig, Turkey

    Eyup Bagci & Emel Aydin

Authors
  1. Lucian Hritcu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eyup Bagci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emel Aydin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marius Mihasan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucian Hritcu.

Ethics declarations

Conflict of interests

The authors have declared that no competing interests exist.

Ethical standard

This study was approved by the Committee on the Ethics of Animal Experiments of the Alexandru Ioan Cuza University of Iasi (Permit Number: 2192) and also, efforts were made to minimize animal suffering and to reduce the number of animals used.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hritcu, L., Bagci, E., Aydin, E. et al. Antiamnesic and Antioxidants Effects of Ferulago angulata Essential Oil Against Scopolamine-Induced Memory Impairment in Laboratory Rats. Neurochem Res 40, 1799–1809 (2015). https://doi.org/10.1007/s11064-015-1662-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-015-1662-6

Keywords

Search

Navigation