Morinda lucida,Peptide extract,Plasmodium berghei,Antioxidant,Oxidative stress," /> Morinda lucida,Peptide extract,Plasmodium berghei,Antioxidant,Oxidative stress,"/> Antioxidant defense system induced by cysteine-stabilized peptide fraction of aqueous extract of <em>Morinda lucida</em> leaf in selected tissues of <em>Plasmodium berghei</em>-infected mice
Search JIM Advanced Search

Journal of Integrative Medicine ›› 2017, Vol. 15 ›› Issue (5): 388-397.doi: 10.1016/S2095-4964(17)60354-6

• Research Article • Previous Articles     Next Articles

Antioxidant defense system induced by cysteine-stabilized peptide fraction of aqueous extract of Morinda lucida leaf in selected tissues of Plasmodium berghei-infected mice

Kayode E. Adewole, Joseph O. Adebayo   

  1. Department of Biochemistry, Faculty of Life Sciences, University of Ilorin, Ilorin 24003, Nigeria
  • Received:2017-01-19 Accepted:2017-04-29 Online:2017-09-15 Published:2017-09-15
  • Contact: Joseph O. Adebayo, Ph.D; E-mail: topebayo2002@yahoo.com

Objective

This study evaluated the responses of some antioxidant parameters in selected tissues of Plasmodium berghei-infected mice treated with cysteine-stabilized peptide fraction (CSPF) of aqueous extract of Morinda lucida leaf.

Methods

Fifty-six mice were randomly divided into seven groups. Group A (normal control) was uninfected and received 5% dimethyl sulfoxide (DMSO). Mice in Groups B (negative control), C, D, E and F were inoculated with P. berghei NK65 and were administered with 5% DMSO and 15.63, 31.25, 61.5 and 125 mg/kg body weight of CSPF respectively. Group G animals, were also inoculated with P. berghei NK65, and received 20 mg/kg body weight of chloroquine. The administration lasted for three days, after which malondialdehyde (MDA) concentration and various antioxidant parameters in selected tissues of mice were determined on days 4 and 8 post-inoculation.

Results

The results revealed that MDA concentration was significantly increased (P < 0.05) in the tissues of the negative control and chloroquine-treated groups. The increased MDA concentration was reduced by CSPF in a dose-dependent manner, which was significant (P < 0.05) at higher doses. The activities of superoxide dismutase, catalase, glutathione peroxidase, glutathione reductase and glutathione-S-transferase and the concentration of reduced glutathione were significantly reduced (P < 0.05) in the tissues of the negative control animals compared to the normal controls. This observed reduction in the negative control animals was reverted in a dose-dependent manner in infected animals given CSPF, even to the range of the normal controls at highest dose, as did chloroquine.

Conclusion

The results suggest that CSPF of M. lucida leaf extract may induce the antioxidant defense system in vivo against Plasmodium species infection.

Key words: Morinda lucida, Peptide extract, Plasmodium berghei, Antioxidant, Oxidative stress

1 1 World Health Organization. World malaria report 2015. (2015-12) [2017-01-19]. . World malaria report 2015. (2015-12) [2017-01-19]. http://www.who.int/malaria/ publications/world-malaria-report-2015/report/en/.
2 Guantai E, Chibale K.How can natural products serve as a viable source of lead compounds for the development of new/novel anti-malarials?Malar J. 2011; 10(Suppl 1): S2.
3 Guerin PJ, Olliaro P, Nosten F, Druilhe P, Laxminaraya R, Binka F, Kilama WL, Ford N, White NJ.Malaria: current status of control, diagnosis, treatment, and a proposed agenda for research and development.Lancet Infec Dis. 2002; 2(9): 564-573.
4 Willcox ML, Bodeker G.Traditional herbal medicines for malaria.BMJ. 2004; 329(7475): 1156-1159.
5 Gründemann C, Thell K, Lengen K, Garcia-Käufer M, Huang YH, Huber R, Craik DJ, Schabbauer1 G, Gruber CW. Cyclotides suppress human T-lymphocyte proliferation by an interleukin 2-dependent mechanism.PLoS One. 2013; 8(6): e68016.
6 Sohail M, Kaul A, Raziuddin M, Adak T.Decreased glutathione-S-transferase activity: diagnostic and protective role in vivax malaria.Clin Biochem. 2007; 40(5-6): 377-382.
7 Atamna H, Ginsburg H.Origin of reactive oxygen species in erythrocytes infected withPlasmodium falciparum. Mol Biochem Parasitol. 1993; 61(2): 231-241.
8 Cabrales P, Zanini GM, Meays D, Frangos JA, Carvalho LJ.Nitric oxide protection against murine cerebral malaria is associated with improved cerebral microcirculatory physiology.J Infect Dis. 2011; 203(10): 1454-1463.
9 Percário S, Moreira DR, Gomes BA, Ferreira ME, Gonçalves AC, Laurindo PS, Vilhena TC, Dolabela MF, Green MD.Oxidative stress in malaria.Int J Mol Sci. 2012; 13(12): 16346-16372.
10 Koehbach J, Attah AF, Berger A, Hellinger R, Kutchan TM, Carpenter EJ, Rolf M, Sonibare MA, Moody JO, Wong GK, Dessein S, Greger H, Gruber CW.Cyclotide discovery in Gentianales revisited—identification and characterization of cyclic cystine-knot peptides and their phylogenetic distribution in Rubiaceae plants.Biopolymers. 2013; 100(5): 438-452.
11 Peters W.Drug resistance in Plasmodium berghei Vinka and Lips.Exp Parasitol. 1965; 17(1): 97-102.
12 Carvalho LH, Krettli AU.Antimalarial chemotherapy with natural products and chemically defined molecules.Mem Inst Oswaldo Cruz. 1991; 86(Suppl 2): 181-184.
13 Ngaha EO, Akanji MA, Madusolomo MA.Studies on correlation between chloroquine-induced tissue damage and serum changes in rats.Experientia. 1982; 45(2): 143-146.
14 Varshney R, Kale RK.Effect of calmodulin antagonist on radiation-induced lipid peroxidation in microsomes.Int J Radiat Biol. 1990; 58(5): 733-743.
15 Sinha AK.Colorimetric assay of catalase.Anal Biochem. 1972; 47(2): 389-394.
16 Misra HP, Fridovich I.The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase.J Biol Chem. 1972; 247(10): 3170-3175.
17 Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG.Selenium: biochemical role as a component of glutathione peroxidase.Science. 1973; 179(4073): 588-590.
18 Carlberg I, Mannervik B.Glutathione reductase.Methods Enzymol. 1985; 113: 484-490.
19 Habig WH, Pabst MJ, Jacoby WB. Glutathione-Stransferases.The first enzymatic step in mercapturic acid formation.J Biol Chem. 1974; 249(22): 7130-7139.
20 Beutler E, Duron O, Kelly BM.Improved method for the determination of blood glutathione.J Lab Clin Med. 1963; 61: 882-888.
21 21 Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tanenbaum SR. Analysis of nitrate, nitrite and [15N] nitrate in biological fluids.Ann Biochem. 1982; 126(1): 131-138.
22 Okeola VO, Adaramoye OA, Nneji CM, Falade CO, Farombi EO, Ademowo OG.Antimalarial and antioxidant activities of methanolic extract ofNigella sativa seeds (black cumin) in mice infected with Plasmodium yoelli nigeriensis. Parasitol Res. 2011; 108(6): 1507-1512.
23 Omonkhua AA, Cyril-Olutayo MC, Akanbi OM, Adebayo OA.Antimalarial, hematological, and antioxidant effects of methanolic extract ofTerminalia avicennioides in Plasmodium berghei-infected mice. Parasitol Res. 2013; 112(10): 3497-3503.
24 24 Gamboa de Domínguez ND, Charris J, Dominguez J, Monasterios M, Angel J, Rodrigues J. Effects of 5,8-dimethylthieno[2,3-b]quinolone-2-carboxylic acid on the antioxidative defense and lipid membranes inPlasmodium berghei-infected erythrocytes. Exp Parasitol. 2015; 155: 26-34.
25 Oluwatosin A, Tolulope A, Ayokulehin K, Patricia O, Aderemi K, Catherine F, Olusegun A.Antimalarial potential of kolaviron, a biflavonoid fromGarcinia kola seeds, against Plasmodium berghei infection in Swiss albino mice. Asian Pac J Trop Med. 2014; 7(2): 97-104.
26 Postma NS, Mommers EC, Eling WM, Zuidema J.Oxidative stress in malaria: implications for prevention and therapy.Pharm World Sci. 1996; 18(4): 121-129.
27 Halliwell B.Biochemistry of oxidative stress.Biochem Soc Trans. 2007; 35(Pt 5): 1147-1150.
28 López-Jaén AB, Valls-Bellésa V, Codoñer-Franch P.Antioxidants: a review.J Pediatric Biochem. 2013; 3(3): 123-128.
29 Zelko IN, Mariani TJ, Folz RJ.Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression.Free Radic Biol Med. 2002; 33(3): 337-349.
30 Hunt NH, Stocker R.Oxidative stress and the redox status of malaria-infected erythrocytes.Blood Cells. 1990; 16(2- 3): 499-526.
31 Raza A, Varshney SK, Khan HM, Malik MA, Mehdi AA, Shukla I.Superoxide dismutase activity in patients of cerebral malaria.Asian Pacific J Trop Dis. 2015; 5(Suppl 1): S51-S53.
32 Chelikani P, Fita I, Loewen PC.Diversity of structures and properties among catalases.Cell Mol Life Sci. 2004; 61(2): 192-208.
33 vander Jagt DL, Hunsaker LA, Campos NM, Scaletti JV. Localization and characterization of haemoglobindegrading aspartic proteinases from the malarial parasitePlasmodium falciparum. Biochim Biophys Acta. 1992; 1122(3): 256-264.
34 Balogun EA, Zailani AH, Adebayo JO. Augmentation of antioxidant system: contribution to antimalarial activity of Clerodendrum violaceum leaf extract. Tang.2014; 4(4): 26.1-26.9.
35 Areekul S, Boonme Y.Catalase activity in red cell and liver of mice infected withPlasmodium berghei. Southeast Asian J Trop Med Public Health. 1986; 17(1): 48-52.
36 Das BS, Nanda NK.Evidence for erythrocyte lipid peroxidation in acute falciparum malaria.Trans R Soc Trop Med Hyg. 1999; 93(1): 58-62.
37 Acharya JD, Ghaskadbi SS.Islets and their antioxidant defense.Islets. 2010; 2(4): 225-235.
38 Araujo CF, Lacerda MV, Abdalla DS, Lima ES.The role of platelet and plasma markers of antioxidant status and oxidative stress in thrombocytopenia among patients with vivax malaria.Mem Inst Oswaldo Cruz. 2008; 103(6): 517-521.
39 Erel O, Vural H, Aksoy N, Aslan G, Ulukanligil M.Oxidative stress of platelets and thrombocytopenia in patients with vivax malaria.Clin Biochem. 2001; 34(4): 341-344.
40 Blum J, Fridovich I.Inactivation of glutathione peroxidase by superoxide radical.Arch Biochem Biophys. 1985; 240(2): 500-508.
41 Tutic M, Lu XA, Schirmer RH, Werner D.Cloning and sequencing of mammalian glutathione reductase cDNA.Eur J Biochem. 1990; 188(3): 523-528.
42 Müller S.Redox and antioxidant systems of the malaria parasitePlasmodium falciparum. Mol Microbiol. 2004; 53(5): 1291-1305.
43 Rodrigues JR, Gamboa ND.Effect of dequalinium on the oxidative stress inPlasmodium berghei-infected erythrocytes. Parasitol Res. 2009; 104(6): 1491-1496.
44 Salinas AE, Wong MG.Glutathione S-transferases—a review.Curr Med Chem. 1999; 6(4): 279-309.
45 Sies H.Glutathione and its role in cellular functions.Free Radic Biol Med. 1999; 27(9-10): 916-921.
46 Lüersen K, Walter RD, Müller S.Plasmodium falciparuminfected red blood cells depend on a functional glutathione de novo synthesis attributable to an enhanced loss of glutathione. Biochem J. 2000; 346(Pt 2): 545-552.
47 Giustarini D, Rossi R, Milzani A, Dalle-Donne I.Nitrite and nitrate measurement by Griess reagent in human plasma: evaluation of interferences and standardization.Methods Enzymol. 2008; 440: 361-380.
48 Kim-Shapiro DB, Gladwin MT.Pitfalls in measuring NO bioavailability using NOx.Nitric Oxide. 2015; 44: 1-2.
49 Ehrhardt S, Mockenhaupt FP, Anemana SD, Otchwemah RN, Wichmann D, Cramer JP, Bienzle U, Burchard GD, Brattig NW.High levels of circulating cardiac proteins indicate cardiac impairment in Africa children with severePlasmodium falciparum malaria. Microbes Infect. 2005; 7(11-12): 1204-1210.
50 Anstey NM, Granger DL, Hassanali MY, Mwaikambo ED, Duffy PE, Weinberg JB.Nitric oxide, malaria, and anemia: inverse relationship between nitric oxide production and hemoglobin concentration in asymptomatic, malariaexposed children.Am J Trop Med Hyg. 1999; 61(2): 249-252.
51 Dhangadamajhi G, Mohapatra BN, Kar SK, Ranjit MR.The CCTTT pentanucleotide microsatellite in iNOS promoter influences the clinical outcome inP. falciparum infection. Parasitol Res. 2009; 104(6): 1315-1320.
52 Hobbs MR, Udhayakumar V, Levesque MC, Booth J, Roberts JM, Tkachuk AN, Pole A, Coon H, Kariuki S, Nahlen BL, Mwaikambo ED, Lal AL, Granger DL, Anstey NM, Weinberg JB.A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children.Lancet. 2002; 360(9344): 1468-1475.
53 Rockett KA, Awburn MM, Cowden WB, Clark IA.Killing ofPlasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun. 1991; 59(9): 3280-3283.
54 Seguin MC1, Klotz FW, Schneider I, Weir JP, Goodbary M, Slayter M, Raney JJ, Aniagolu JU, Green SJ. Induction of nitric oxide synthase protects against malaria in mice exposed to irradiatedPlasmodium berghei infected mosquitoes: involvement of interferon gamma and CD8+ T cells. J Exp Med. 1994; 180(1): 353-358.
55 Ong PK, Melchior B, Martins YC, Hofer A, Orjuela- Sánchez P, Cabrales P, Zanini GM, Frangos JA, Carvalho LJ.Nitric oxide synthase dysfunction contributes to impaired cerebroarteriolar reactivity in experimental cerebral malaria.PLoS Pathog. 2013; 9(6): e1003444.
56 Gramaglia I, Sobolewski P, Meays D, Contreras R, Nolan JP, Frangos JA, van der Heyde HC. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria.Nat Med. 2006; 12(12): 1417-1422.
57 Jeney V, Ramos S, Bergman ML, Bechmann I, Tischer J, Ferreira A, Oliveira-Marques V, Janse CJ, Rebelo S, Cardoso S, Soares MP.Control of disease tolerance to malaria by nitric oxide and carbon monoxide.Cell Rep. 2014; 8(1): 126-136.
[1] Dona Nirmani Ann Wijewickrama Samarakoon, Deepthi Inoka Uluwaduge, Malith Aravinda Siriwardhene. Mechanisms of action of Sri Lankan herbal medicines used in the treatment of diabetes: A review. Journal of Integrative Medicine, 2020, 18(1): 13-20.
[2] Gerli E.G. Herr, Fábio Goulart da Silva, Francisco José Cidral-Filho, Fabricia Petronilho, Lucinéia Gainski Danielski, Mariana Pereira de Souza Goldim, Afonso Shiguemi Inoue Salgado, Franciane Bobinski, Daniel Fernandes Martins, Eliane R. Winkelmann. Effects of the use of bioceramic wraps in patients with lower limb venous ulcers: A randomized double-blind placebo-controlled trial. Journal of Integrative Medicine, 2020, 18(1): 27-.
[3] Syed Fairus, Hwee Ming Cheng, Kalyana Sundram. Antioxidant status following postprandial challenge of two different doses of tocopherols and tocotrienols. Journal of Integrative Medicine, 2020, 18(1): 68-79.
[4] Gaëtan Olivier Fankem, Michel Archange Fokam Tagne, Paul Aimé Noubissi, Angèle Foyet Fondjo, Idrice Kamtchouing, Adela Ngwewondo, Henri Wambe, Joseph Ngakou Mukam, René Kamgang. Antioxidant activity of dichloromethane fraction of Dichrocephala integrifolia in Salmonella typhi-infected rats. Journal of Integrative Medicine, 2019, 17(6): 438-445.
[5] Rabie Kachkoul, Tarik Squalli Housseini, Mohamed Mohim, RadouaneEl Habbani, Youssef Miyah, Anissa Lahrichi. Chemical compounds as well as antioxidant and litholytic activities of Arbutus unedo L. leaves against calcium oxalate stones. Journal of Integrative Medicine, 2019, 17(6): 430-437.
[6] Álisson de Carvalho Gonçalves, Einy Jéssika Siqueira Moreira, Guilherme Vannucchi Portari. Benfotiamine supplementation prevents oxidative stress in anterior tibialis muscle and heart. Journal of Integrative Medicine, 2019, 17(6): 423-429.
[7] Pranay Soni, Rajesh Choudhary, Surendra H. Bodakhe. Effects of a novel isoflavonoid from the stem bark of Alstonia scholaris against fructose-induced experimental cataract. Journal of Integrative Medicine, 2019, 17(5): 374-382.
[8] Fang-yuan Wang, Jian Jia, Huan-huan Song, Cheng-ming Jia, Chang-bo Chen, Jing Ma. Icariin protects vascular endothelial cells from oxidative stress through inhibiting endoplasmic reticulum stress. Journal of Integrative Medicine, 2019, 17(3): 205-212.
[9] Fatma Mohamed Hussein Shediwah, Khalid Mohammed Naji, Hussein Saleh Gumaih, Fatima A Alhadi, Amani Lutf Al-Hammami, Myrene Roselyn D'Souza. Antioxidant and antihyperlipidemic activity of Costus speciosus against atherogenic diet-induced hyperlipidemia in rabbits. Journal of Integrative Medicine, 2019, 17(3): 181-191.
[10] Lucky Legbosi Nwidu, Yibala Ibor Oboma. Telfairia occidentalis (Cucurbitaceae) pulp extract mitigates rifampicin-isoniazid-induced hepatotoxicity in an in vivo rat model of oxidative stress. Journal of Integrative Medicine, 2019, 17(1): 46-56.
[11] Khaled M. M. Koriem, Mahmoud S. Arbid, Hend N. Saleh . Antidiarrheal and protein conservative activities of Psidium guajava in diarrheal rats. Journal of Integrative Medicine, 2019, 17(1): 57-65.
[12] The Su Moe, Htet Htet Win, Thin Thin Hlaing, War War Lwin, Zaw Min Htet, Khin Mar Mya . Evaluation of in vitro antioxidant, antiglycation and antimicrobial potential of indigenous Myanmar medicinal plants. Journal of Integrative Medicine, 2018, 16(5): 358-366.
[13] Carola Analía Torres, Cristina Marisel Pérez Zamora, María Beatriz Nuñez, Ana María Gonzalez. In vitro antioxidant, antilipoxygenase and antimicrobial activities of extracts from seven climbing plants belonging to the Bignoniaceae. Journal of Integrative Medicine, 2018, 16(4): 255-262.
[14] Omar Farid, Farid Khallouki, Morad Akdad, Andrea Breuer, Robert Wyn Owen, Mohamed Eddouks. Phytochemical characterization of polyphenolic compounds with HPLC–DAD–ESI–MS and evaluation of lipid-lowering capacity of aqueous extracts from Saharan plant Anabasis aretioides (Coss & Moq.) in normal and streptozotocin-induced diabetic rats. Journal of Integrative Medicine, 2018, 16(3): 185-191.
[15] Akintayo Lanre Ogundajo, Lateef Apollo Adeniran, Anofi Omotayo Ashafa. Medicinal properties of Ocotea bullata stem bark extracts: Phytochemical constituents, antioxidant and anti-inflammatory activity, cytotoxicity and inhibition of carbohydrate-metabolizing enzymes. Journal of Integrative Medicine, 2018, 16(2): 132-140.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Jin-zhou Tian, Jing Shi, Xin-qing Zhang, Qi Bi, Xin Ma, Zhi-liang Wang, Xiao-bin Li, Shu-li Shen, Lin Li, Zhen-yun Wu, Li-yan Fang, Xiao-dong Zhao, Ying-chun Miao, Peng-wen Wang, Ying Ren, Jun-xiang Yin, Yong-yan Wang, Beijing United Study Group on MCI of the Capital Foundation of Medical Developments. An explanation on "guiding principles of clinical research on mild cognitive impairment (protocol)". Journal of Chinese Integrative Medicine, 2008, 6(1): 15-21
[2] Dong Yang, Yong-ping Du, Qing Shen, Wei Chen, Yan Yu, Guang-lei Chen. Expression of alpha-smooth muscle actin in renal tubulointerstitium in patients with kidney collateral stasis. Journal of Chinese Integrative Medicine, 2008, 6(1): 41-44
[3] Zhi-chun Jin. Problems in establishing clinical guideline for integrated traditional Chinese and Western medicine. Journal of Chinese Integrative Medicine, 2008, 6(1): 5-8
[4] SUN Ming-yu, ZUO Jian, DUAN Ji-feng, HAN Jun, FAN Shi-ming, ZHANG Wei, ZHU Li-fang, YAO Ming-hui. Antitumor activities of kushen flavonoids in vivo and in vitro. Journal of Chinese Integrative Medicine, 2008, 6(1): 51-59
[5] Min Cheng, Qiong Feng, Shu-wen Qian, Hui Gao, Cui-qing Zhu. Preliminary assay of p-amyloid binding elements in heart-beneficial recipe. Journal of Chinese Integrative Medicine, 2008, 6(1): 68-72
[6] Hai-feng Wei, Bai-liu Ya, Ling Zhao, Cui-fei Ye, Li Zhang, Lin Li. Evaluation of tongue manifestation of blood stasis syndrome and its relationship with blood rheological disorder in a rat model of transient brain ischemia. Journal of Chinese Integrative Medicine, 2008, 6(1): 73-76
[7] Guo-hong Yuan, Xiao-jing Pang, He-chao Ma. Synergic effects of Danggui Buxue Decoction in reducing toxicity of cytoxan in tumor-bearing mice. Journal of Chinese Integrative Medicine, 2008, 6(1): 83-88
[8] Bing Hu , Hong-mei An , Ke-ping Shen , Qin Du. Senescence-inducing effects of Chinese herbal medicine Tenglong Buzhong Decoction on human colon carcinoma LS-174-T cells and the mechanism. Journal of Chinese Integrative Medicine, 2010, 8(11): 1048-1052
[9] Jing-yuan Mao, Chang-xiao Liu, Heng-he Wang, Guang-li Wei , Zhen-peng Zhang, Jie Xing, Wang Xian liang , Ying-fei Bi . Effects of Shenmai Injection on serum concentration and pharmacokinetics of digoxin in dogs with heart failure. Journal of Chinese Integrative Medicine, 2010, 8(11): 1070-1074
[10] Chan Chen, Yong-mei Meng , Peng Zhang, Juan Wang, Hui-hui Zhao, Shu-zhen Guo , Wei Wang. Diagnosis and treatment rule of traditional Chinese medicine for syndrome factors of chronic congestive heart failure: a study based on Shannon entropy method. Journal of Chinese Integrative Medicine, 2010, 8(11): 1080-1084