Prevention of short-term memory impairment by Bryophyllum pinnatum (Lam.) Oken and its effect on acetylcholinesterase changes in CCl4-induced neurotoxicity in rats

Scholastica Onyebuchi Anadozie; Jacob Ayodele Akinyemi; Olusola Bolaji Adewale; Christy Chinwe Isitua

doi:10.1515/jbcpp-2018-0161

Article

Prevention of short-term memory impairment by Bryophyllum pinnatum (Lam.) Oken and its effect on acetylcholinesterase changes in CCl₄-induced neurotoxicity in rats

Scholastica Onyebuchi Anadozie , Jacob Ayodele Akinyemi , Olusola Bolaji Adewale and Christy Chinwe Isitua

Published/Copyright: September 9, 2019

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From the journal Journal of Basic and Clinical Physiology and Pharmacology Volume 30 Issue 5

Abstract

Background

Short-term memory impairment is a neurodegenerative disease associated with oxidative stress. Bryophyllum pinnatum (Lam.) Oken of the family Crassulaceae is traditionally used in the treatment of diseases, such as cough, wounds, and kidney diseases. This study evaluates the effect of the aqueous extract of B. pinnatum (AEBP) leaves on acetylcholinesterase activity in carbon tetrachloride (CCl₄)-induced short-term memory impairment in rats.

Methods

Thirty male Wistar albino rats were used in this study and were divided into six groups (n=5). Group I served as control, group II rats were induced with CCl₄, while groups III–V animals were pretreated with silymarin (25 mg/kg body weight), 25 and 50 mg/kg body weight AEBP leaves, respectively, once daily by oral gavage for 14 days prior to a single intraperitoneal injection of CCl₄. Animals in group VI received 50 mg/kg body weight AEBP only by oral gavage.

Results

Administration of carbon tetrachloride significantly increased (p<0.05) spontaneous alternation and locomotor function in rats when compared with the control group. Also, the levels of acetylcholinesterase, adenosine deaminase, and malondialdehyde were increased in CCl₄-administered rats, with reduction in both enzymatic and nonenzymatic antioxidant levels. However, pretreatment of rats with AEBP leaves, at tested doses, prevented these changes.

Conclusions

The increased antioxidant status and the inhibition of acetylcholinesterase activity show that AEBP leaves improve learning memory and stabilizes memory impairment caused by CCl₄.

Keywords: acetylcholinesterase; antioxidant; Bryophyllum pinnatum; carbon tetrachloride; degenerative diseases; oxidative stress

Acknowledgments

The authors thank the management of Afe Babalola University, Ado-Ekiti for providing support in terms of facilities.

Author contributions: All the authors took part actively in every aspect of the research and preparation of this article and as such accepted responsibility for the entire content of the submitted manuscript.S.O Anadozie conducted the research and prepared the manuscript, J.A Akinyemi designed the study and provided chemicals used for the research, O.B Adewale performed the statistical analysis and profreading of the manuscript, C.C Isitua assited in obtaining ethical clearance on the study and revised the manuscript
Research funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Employement or leadership: None declared.
Honorarium: None declared.
Competing interests: The authors declare that there are no conflicts of interest with respect to the research, authorship, and/or publication of this article.
Ethica approval: Research involving animals complies with all relevant national regulations and institutional policies (NIH Publication, revised in 1985) for the care and use of animals. The ethical committee of Afe Babalola University approval the ues of animal in this study with ethical number ABUAD-SCI04/03/16/012.

References

[1] Weber LW, Boll M, Stampfl A. Hepatotoxicity and mechanism of action of haloalkanes: Carbon tetrachloride as a toxicological model. Crit Rev Toxicol 2003;33:105–36.10.1080/713611034Search in Google Scholar

[2] Alkreathy HM, Khan RA, Khan MR, Sahreen S. CCl₄ induced genotoxicity and DNA oxidative damages in rats: hepatoprotective effect of Sonchus arvensis. BMC Complement Altern Med 2014;14:452.10.1186/1472-6882-14-452Search in Google Scholar

[3] Wallace AD. Toxic endpoints in the study of human exposure to environmental chemicals. Prog Mol Biol Transl Sci 2012;112:89–115.10.1016/B978-0-12-415813-9.00004-0Search in Google Scholar

[4] Ware GW. Carbon tetrachloride. In: Reviews of environmental contamination and toxicology. New York: Springer, 1988;21–35.10.1007/978-1-4612-3922-2_3Search in Google Scholar

[5] Adewale OB, Onasanya A, Anadozie SO, Ogbole CJ, Akintan IA, Abu MF. Protective effect of ethanolic extract of Crassocephalum rubens leaves on carbon tetrachloride-induced liver damage in rats. World J Pharm Med Res 2015;4:156–68.Search in Google Scholar

[6] Khan RA, Khan MR, Sahreen S. CCl₄-induced hepatotoxicity: protective effect of rutin on p53, CYP2E1 and the antioxidative status in rat. BMC Complement Altern Med 2012;12:178.10.1186/1472-6882-12-178Search in Google Scholar

[7] Ferrier D. The functions of the brain. New York: G. P. Putnam’s Sons, 1886.Search in Google Scholar

[8] Frackowiak RS, Friston KJ, Frith C, Dolan R, Price CJ, Zeki S, et al. Human brain function, 2nd ed. Cambridge, MA: Academic Press, 2003.Search in Google Scholar

[9] Bhat AH, Dar KB, Anees S, Zargar MA, Masood A, Sofi MA, et al. Oxidative stress, mitochondrial dysfunction and neurodegenerative diseases; a mechanistic insight. Biomed Pharmacother 2015;74:101–10.10.1016/j.biopha.2015.07.025Search in Google Scholar

[10] Friedman J. Why is the nervous system vulnerable to oxidative stress? In: Oxidative stress and free radical damage in neurology. New York: Springer, 2011;19–27.10.1007/978-1-60327-514-9_2Search in Google Scholar

[11] Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009;7:65–74.10.2174/157015909787602823Search in Google Scholar

[12] Esposito E, Rotilio D, Di Matteo V, Di Giulio C, Cacchio M, Algeri S. A review of specific dietary antioxidants and the effects on biochemical mechanisms related to neurodegenerative processes. Neurobiol Aging 2002;23:719–35.10.1016/S0197-4580(02)00078-7Search in Google Scholar

[13] Kumar GP, Khanum F. Neuroprotective potential of phytochemicals. Pharmacogn Rev 2012;6:81–90.10.4103/0973-7847.99898Search in Google Scholar PubMed PubMed Central

[14] Gill LS. Ethnomedical uses of plants in Nigeria. Benin: Uniben Press, 1992:275.Search in Google Scholar

[15] Salami SS, Schmidt F, Laxman B, Regan MM, Rickman DS, Scherr D, et al., editors. Combining urinary detection of TMPRSS2:ERG and PCA3 with serum PSA to predict diagnosis of prostate cancer. Urol Oncol 2013;31:566–71.10.1016/j.urolonc.2011.04.001Search in Google Scholar PubMed PubMed Central

[16] Anadozie SO, Akinyemi JA, Agunbiade S, Ajiboye BO, Adewale OB. Bryophyllum pinnatum inhibits arginase II activity and prevents oxidative damage occasioned by carbon tetrachloride (CCl₄) in rats. Biomed Pharmacother 2018;101:8–13.10.1016/j.biopha.2018.01.156Search in Google Scholar

[17] Pattewar SV. Kalanchoe pinnata: phytochemical and pharmacological profile. Int J Pharm Sci Res 2012;3:993.10.7439/ijpp.v2i1.223Search in Google Scholar

[18] Ojewole JA. Antinociceptive, anti-inflammatory and antidiabetic effects of Bryophyllum pinnatum (Crassulaceae) leaf aqueous extract. J Ethnopharmacol 2005;99:13–9.10.1016/j.jep.2005.01.025Search in Google Scholar

[19] Adenike K, Eretan OB. Purification and partial characterization of a lectin from the fresh leaves of Kalanchoe crenata (Andr.) Haw. J Biochem Mol Biol 2004;37:229–33.10.5483/BMBRep.2004.37.2.229Search in Google Scholar

[20] Beppe GJ, Dongmo AB, Foyet HS, Tsabang N, Olteanu Z, Cioanca O, et al. Memory-enhancing activities of the aqueous extract of Albizia adianthifolia leaves in the 6-hydroxydopamine-lesion rodent model of Parkinson’s disease. BMC Complement Altern Med 2014;14:142.10.1186/1472-6882-14-142Search in Google Scholar

[21] Seibenhener ML, Wooten MC. Use of the Open Field Maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp 2015;6:52434.10.3791/52434Search in Google Scholar

[22] Ellman GL, Courtney KD, Andres V, Jr., Feather-Stone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961;7:88–95.10.1016/0006-2952(61)90145-9Search in Google Scholar

[23] Giusti G. Adenosine deaminase A2. In: Bergmeyer HU, editor. Methods of enzymatic analysis, 2nd ed. Cambridge, MA: Academic Press, 1974:1092–9.10.1016/B978-0-12-091302-2.50108-0Search in Google Scholar

[24] Alía M, Horcajo C, Bravo L, Goya L. Effect of grape antioxidant dietary fiber on the total antioxidant capacity and the activity of liver antioxidant enzymes in rats. Nutr Res 2003;23:1251–67.10.1016/S0271-5317(03)00131-3Search in Google Scholar

[25] Sinha AK. Colorimetric assay of catalase. Anal Biochem 1972;47:389–94.10.1016/0003-2697(72)90132-7Search in Google Scholar

[26] Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959;82:70–7.10.1016/0003-9861(59)90090-6Search in Google Scholar

[27] Morakinyo AO, Adeniyi OS, Arikawe AP. Effects of Zingiber officinale on reproductive functions in the male rat. Afr J Biomed Res 2008;11:329–34.10.4314/ajbr.v11i3.50750Search in Google Scholar

[28] Varshney R, Kale R. Effects of calmodulin antagonists on radiation-induced lipid peroxidation in microsomes. Int J Radiat Biol 1990;58:733–43.10.1080/09553009014552121Search in Google Scholar PubMed

[29] Parthasarathy A. Partha’s 101 clinical pearls in pediatrics. New Delhi: Jaypee Brothers, Medical Publishers Pvt. Limited, 2017.Search in Google Scholar

[30] Pal PB, Pal S, Manna P, Sil PC. Traditional extract of Pithecellobium dulce fruits protects mice against CCl₄ induced renal oxidative impairments and necrotic cell death. Pathophysiology 2012;19:101–14.10.1016/j.pathophys.2012.02.001Search in Google Scholar PubMed

[31] Sayre LM, Perry G, Smith MA. Oxidative stress and neurotoxicity. Chem Res Toxicol 2008;21:172–88.10.1021/tx700210jSearch in Google Scholar PubMed

[32] Subash S, Essa MM, Al-Adawi S, Memon MA, Manivasagam T, Akbar M. Neuroprotective effects of berry fruits on neurodegenerative diseases. Neural Regen Res 2014;9:1557–66.10.4103/1673-5374.139483Search in Google Scholar PubMed PubMed Central

[33] Adeniyi PA, Ishola AO, Laoye BJ, Olatunji BP, Bankole OO, Shallie PD, et al. Neural and behavioural changes in male periadolescent mice after prolonged nicotine-MDMA treatment. Metabolic Brain Dis 2016;31:93–107.10.1007/s11011-015-9691-zSearch in Google Scholar PubMed

[34] Kwon S-H, Ma S-X, Joo H-J, Lee S-Y, Jang C-G. Inhibitory effects of Eucommia ulmoides Oliv. bark on scopolamine-induced learning and memory deficits in mice. Biomol Ther 2013;21:462–9.10.4062/biomolther.2013.074Search in Google Scholar PubMed PubMed Central

[35] Garry PS, Ezra M, Rowland MJ, Westbrook J, Pattinson KT. The role of the nitric oxide pathway in brain injury and its treatment – from bench to bedside. Exp Neurol 2015;263:235–43.10.1016/j.expneurol.2014.10.017Search in Google Scholar PubMed

[36] Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 1995;57:683–706.10.1146/annurev.ph.57.030195.003343Search in Google Scholar PubMed

[37] Hannibal L. Nitric oxide homeostasis in neurodegenerative diseases. Curr Alzheimer Res, 2016;13:135–49.10.2174/1567205012666150921101250Search in Google Scholar PubMed

[38] Karadeniz A, Yildirim A, Çelebi F. Protective effect of Panax ginseng against carbon tetrachloride (CCl₄)-induced oxidative brain injury in rats. Atatürk Üni Vet Bil Derg 2007;2:117–21.Search in Google Scholar

[39] Ismail A, Essawy MM, Salem AA. Protective effect of grape seed oil against CCl₄ induced oxidative stress in rat brain. J Agric Chem Biotechn 2014;5:281–303.10.21608/jacb.2014.50047Search in Google Scholar

[40] Shah AS, Ahmed M, Alkreathy HM, Khan MR, Khan RA, Khan S. Phytochemical screening and protective effects of Trifolium alexandrinum (L.) against free radical-induced stress in rats. Crit Rev Food Sci Nutr 2014;2:751–7.10.1002/fsn3.152Search in Google Scholar PubMed PubMed Central

[41] Ighodaro OMA, Akinloye O. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alex J Med 2017;10:1111–6.10.1016/j.ajme.2017.09.001Search in Google Scholar

[42] Wessler I, Kirkpatrick CJ. Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans. Br J Pharmacol 2008;154:1558–71.10.1038/bjp.2008.185Search in Google Scholar PubMed PubMed Central

[43] Chinthu R, Anju TR, Paulose CS. Cholinergic receptor alterations in the cerebral cortex of spinal cord injured rat. Biochem Biophys Rep 2017;10:46–51.10.1016/j.bbrep.2017.02.003Search in Google Scholar PubMed PubMed Central

[44] Lovinger DM. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 2010;58:951–61.10.1016/j.neuropharm.2010.01.008Search in Google Scholar PubMed PubMed Central

[45] Ogunruku OO, Oboh G, Ademosun AO. Water extractable phytochemicals from peppers (Capsicum spp.) inhibit acetylcholinesterase and butyrylcholinesterase activities and prooxidants induced lipid peroxidation in rat brain in vitro. Int J Food Sci 2014;2014:605618.10.1155/2014/605618Search in Google Scholar PubMed PubMed Central

[46] Sheth S, Brito R, Mukherjea D, Rybak LP, Ramkumar V. Adenosine receptors: expression, function and regulation. Int J Mol Sci 2014;15:2024–52.10.3390/ijms15022024Search in Google Scholar PubMed PubMed Central

[47] Sachdeva S, Gupta M. Adenosine and its receptors as therapeutic targets: an overview. Saudi Pharm J 2013;21:245–53.10.1016/j.jsps.2012.05.011Search in Google Scholar PubMed PubMed Central

[48] Bauerle JD, Grenz A, Kim JH, Lee HT, Eltzschig HK. Adenosine generation and signaling during acute kidney injury. J Am Soc Nephrol 2011;22:14–20.10.1681/ASN.2009121217Search in Google Scholar PubMed

Received: 2018-08-31

Accepted: 2019-05-22

Published Online: 2019-09-09

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Articles in the same Issue

https://doi.org/10.1515/jbcpp-2018-0161

Keywords for this article

acetylcholinesterase; antioxidant; Bryophyllum pinnatum; carbon tetrachloride; degenerative diseases; oxidative stress