Bioassay-guided isolation and characterization of active antiplasmodial compounds from Murraya koenigii extracts against Plasmodium falciparum and Plasmodium berghei

Parasitology Research

Volumn 113, Issue 5, 2014, Pages 1657-1672

  Kamaraj, Chinnaperumal ^a   Rahuman, Abdul Abdul ^a   Roopan, Selvaraj Mohana ^b   Bagavan, Asokan ^a   Elango, Gandhi ^a   Zahir, Abdul Abduz ^a   Rajakumar, Govindasamy ^a   Jayaseelan, Chidambaram ^a   Santhoshkumar, Thirunavukkarasu ^a   Marimuthu, Sampath ^a   Kirthi, Arivarasan Vishnu ^a  

^a C ABDUL HAKEEM COLLEGE   (India)

^b VIT UNIVERSITY   (India)

Author keywords

Ethyl acetate extract; Malaria; Murraya koenigii

Indexed keywords

ACETIC ACID ETHYL ESTER; CARYOPHYLLENE; CHLOROQUINE; MURRAYA KOENIGII EXTRACT; MYRISTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL ACTIVITY; ANTIMALARIAL DRUG SUSCEPTIBILITY; ARTICLE; BIOASSAY; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DRUG ISOLATION; DRUG PURIFICATION; ERYTHROCYTE; FEMALE; HELA CELL LINE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROSCOPY; LIVER INJURY; LIVER PROTECTION; MALARIA FALCIPARUM; MALE; MOUSE; NEPHROTOXICITY; NONHUMAN; PARASITEMIA; PLANT LEAF; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RENAL PROTECTION; SPLEEN CELL;

ANIMALS; ANTIMALARIALS; FEMALE; HELA CELLS; HUMANS; MALARIA; MALE; MICE; MURRAYA; MYRISTIC ACID; PLANT EXTRACTS; PLANT LEAVES; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; SESQUITERPENES;

EID: 84901370099     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-014-3810-3     Document Type: Article

References (79)

1. Adebajo AC, Olayiwola G, Verspohl JE, Iwalewd EO, Omisore NOA, Bergenthal D (2004) Evaluation of the ethnomedical claims of Murraya koenigii. Pharm Biol 42:610-620
2. Adewoye EO, Salami AT, Taiwo VO (2010) Anti-plasmodial and toxicological effects of methanolic bark extract of Chrysophyllum albidum in albino mice. J Physiol Pathophysiol 1(1):1-9
3. Agarwal HK, Chhikara BS, Bhavaraju S, Mandal D, Doncel GF, Parang K (2013) Emtricitabine prodrugs with improved anti-HIV activity and cellular uptake. Mol Pharm 10(2):467-476
4. Alma MH, Mavi A, Yildirim A, Digrak M, Hirata T (2003) Screening chemical composition and in vitro antioxidant and antimicrobial activities of the essential oils from Origanum syriacum L. growing in Turkey. Biol Pharm Bull 26:1725-1729
5. Arulselvan P, Subramanian SP (2007) Beneficial effects of Murraya koenigii leaves on antioxidant defense system and ultrastructural changes of pancreatic b-cell in experimental diabetes. Chem Biol Interact 165:155-164
6. Bagavan A, Rahuman AA, Kamaraj C, Geetha K (2008) Larvicidal activity of saponin from Achyranthes aspera against Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 103(1):223-229
7. Bagavan A, Rahuman AA, Kamaraj C, Kaushik NK, Mohanakrishnan D, Sahal D (2011a) Antiplasmodial activity of botanical extracts against Plasmodium falciparum. Parasitol Res 108:1099-1109
8. Bagavan A, Rahuman AA, Kaushik NK, Sahal D (2011b) In vitro antimalarial activity of medicinal plant extracts against Plasmodium falciparum. Parasitol Res 108:15-22
9. Bero J, Quetin-Leclercq J (2011) Natural products and tropical diseases. Planta Med 77:571
10. Bhat GP, Surolia N (2001) In vitro antimalarial activity of three plants used in the traditional medicine of India. Am J Trop Med Hyg 65(4):304-308
11. Carrara IV, Zwang J, Asley AE, Price RA, Stepniewka K, Barends M, Brock-man A, Anderson T, McGready R, Phaiphun L, Proux S, Vugt M, van Hutagalung R, Lwin MK, PyaePhyo A, Preechapornkul P, Imwong M, Pukrittayakamee S, Singhasivanon P, White NJ, Nosten F (2009) Changes in the treatment response to artesunate-mefloquine on the north western border of Thailand during 13 years of continuous deployment. PLoS ONE 4:2
12. Chowdhury JU, Bhuiyan MNI, Yusuf M (2008) Chemical composition of the essential oils of Murraya koenigii (L.) Spreng and Murraya paniculata (L.) Jack. Bangladesh J Pharmacol 3:59-63
13. Cornwell PA, Barry BW (1994) Sesquiterpene components of volatile oils as skin penetration enhancers for the hydrophilic permeant 5-fluorouracil. J Pharm Pharmacol 46:261-269
14. David AF, Philip JR, Simon RC, Reto B, Solomon N (2004) Antimalarial drug discovery: efficiency models for compound screening. Nat Rev 3:509-520
15. Dondorp AM, Yeung S, Ngguonn C, Day NP, Socheat D, VonSeidlein L (2010) Artemisinin resistance: current status and scenarios for containment. Nat Rev Microbiol 8:272-280
16. Doria GA, Silva WJ, Carvalho GA, Alves PB, Cavalcanti SC (2010) A study of the larvicidal activity of two Croton species from northeastern Brazil against Aedes aegypti. Pharm Biol 48(6):615-620
17. Dorin D, Le Roch K, Sallicandro P, Alano P, Parzy D, Poullet P, Meijer L, Doerig C (2001) Pfnek-1, a NIMA-related kinase from the human malaria parasite Plasmodium falciparum. Biochemical properties and possible involvement in MAPK regulation. Eur J Biochem 268:2600-2608
18. Ene AC, Atawodi SE, Ameh DA, Kwanshie HO, Agomo PU (2008) Experimental induction of chloroquine resistance in Plasmodium berghei NK 65. Trends Med Res 3(1):16-23
19. George BO, Osioma E, Okpoghono J, Aina OO (2011) Changes in liver and serumtransaminases and alkaline phosphatase enzyme activities in Plasmodium berghei infectedmice treated with aqueous extract of Aframomum sceptrum. Afr J Biochem Res 5(9):277-281
20. Ginsburg H, Deharo E (2011) A call for using natural compounds in the development of new antimalarial treatment an introduction. Malar J 10(Suppl 1):S1
21. Greenwood BM, Bojang K, Whitty CJM, Targett GAT (2005) Malaria. Lancet 365:1487-1498
22. Gupta P, Vasudeva N (2010) In vitro antiplasmodial and antimicrobial potential of Tagetes erecta roots. Pharm Biol 48(11):1218-1223
23. Gurib-Fakim A (2006)Medicinal plants: tradition of yesterday and drugs of tomorrow. Mol Asp Med 27:1-93
24. Iwalewa EO, Oguntoye L, Rai PP, Iyaniwura TT (1997) In vivo and in vitro antimalarial activity of two crude extracts of Cassia occidentalis leaf. Niger J Pharm Sci 5:23-28
25. Kamaraj C, Kaushik NK, Mohanakrishnan D, Elango G, Bagavan A, Zahir AA, Rahuman AA, Sahal D (2012a) Antiplasmodial potential of medicinal plant extracts from Malaiyur and Javadhu hills of South India. Parasitol Res 111(2):703-715
26. Kamaraj C, Kaushik NK, Rahuman AA, Mohanakrishnan D, Bagavan A, Elango G, Zahir AA, Santhoshkumar T, Marimuthu S, Jayaseelan C, Kirthi AV, Rajakumar G, Velayutham K, Sahal D (2012b) Antimalarial activities of medicinal plants traditionally used in the villages of Dharmapuri regions of South India. J Ethnopharmacol 141(3):796-802
27. Kaushik NK, Bagavan A, Rahuman AA, Mohanakrishnan D, Kamaraj C, Elango G, Zahir AA, Sahal D (2013) Antiplasmodial potential of selected medicinal plants from eastern Ghats of South India. Exp Parasitol 134(1):26-32
28. Keluskar P, Ingle S (2012) Ethnopharmacology guided screening of traditional Indian herbs for selective inhibition of Plasmodium specific lactate dehydrogenase. J Ethnopharmacol 144:201-207
29. Khan BA, Abraham A, Leelamma S (1995) Haematological and histological studies after curry leaf (Murraya koenigii) & mustard (Brassica juncea) feeding in rats. Indian J Med Res 102:184-186
30. Khaomek P, Ichino C, Ishiyama A, Sekiguchi H, Namatame M, Ruangrungsi N, Saifah E, Kiyohara H, Otoguro K, Omura S, Yamada H (2008) In vitro antimalarial activity of prenylated flavonoids from Erythrina fusca. J Nat Med 62(2):217-220
31. Kubo I, Chaudhuri SK, Kubo Y, Sanchez Y, Ogura T, Saito T, Ishikawa H, Haraguchi H (1996) Cytotoxic and antioxidative sesquiterpenoids from Heterotheca inuloides. Planta Med 62:427-430
32. Kumari P, Sahal D, Jain SK, Chauhan VS (2012) Bioactivity guided fractionation of leaves extract of Nyctanthes arbor tristis (Harshringar) against P. falciparum. PLoS One 7(12):e51714
33. Lee SJ, Park WH, Moon HI (2009) Bioassay-guided isolation of antiplasmodial anacardic acids derivatives from the whole plants of Viola websteri Hemsl. Parasitol Res 104(2):463-466
34. Li X, Rieckmann K (1992) A bioassay for derivatives of qinghaosu (artemisinin). Trop Med Parasitol 43:195-196
35. Li JWH, Vederas JC (2009) Drug discovery and natural products: end of an era or an endless frontier? Science 325:161-165
36. Li Q, Xie LH, Johnson TO, Si Y, Haeberle AS, Weina PJ (2007) Toxicity evaluation of artesunate and artelinate in Plasmodium berghei-infected and uninfected rats. Trans R Soc Trop Med Hyg 101(2):104-112
37. Liu CH, Huang HY (2012) Antimicrobial activity of curcumin-loaded myristic acid microemulsions against Staphylococcus epidermidis. Chem Pharm Bull (Tokyo) 60(9):1118-1124
38. Lourens AC, Reddy D, Baser KH, Viljoen AM, Van Vuuren SF (2004) In vitro biological activity and essential oil composition of four indigenous South African Helichrysum species. J Ethnopharmacol 95:253-258
39. Macleod JK, Rasmussen HB (1999) A hydroxy-β-caryophyllene from Pterocaulon serrulatum. Phytochem 50:105-108
40. Malwal M, Sarin R (2010) Chemical characterization and antimicrobial screening of volatile components of Murraya koenigii (L.) Spreng - an Indian aromatic tree. J Pharm Res 3(8):1782-1784
41. Mathew N, Ayyanar E, Shanmugavelu S, Muthuswamy K (2013) Mosquito attractant blends to trap host seeking Aedes aegypti. Parasitol Res 112(3):1305-1312
42. Moore BR, Jago JD, Batty KT (2008) Plasmodium berghei: parasite clearance after treatment with dihydroartemisinin in an asplenic murine malaria model. Exp Parasitol 118:458-467
43. Morais TR, Romoff P, Fávero OA, Reimão JQ, Lourenço WC, Tempone AG, Hristov AD, Di Santi SM, Lago JH, Sartorelli P, Ferreira MJ (2012) Anti-malarial, anti-trypanosomal, and anti-leishmanial activities of jacaranone isolated from Pentacalia desiderabilis (Vell.) Cuatrec. (Asteraceae). Parasitol Res 110(1):95-101
44. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63
45. Mueller D, Davis RA, Duffy S, Avery VM, Camp D, Quinn RJ (2009) Antimalarial activity of azafluorenone alkaloids from the Australian tree Mitrephora diversifolia. J Nat Prod 72(8):1538-1540
46. st century. In: Razum O (ed) Malaria in Africa, vol 60. Peter Lang, Frankfurt, p 193
47. Ndjonka D, Bergmann B, Agyare C, Zimbres FM, Luersen K, Hensel A, Wrenger C, Liebau E (2012) In vitro activity of extracts and isolated polyphenols from West African medicinal plants against Plasmodium falciparum. Parasitol Res 111(2):827-834
48. Newman DJ, Cragg GM (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75:311-335
49. Noedl H, Se Y, Socheat D, Fukuda M (2008) Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 359:2619-2620
50. Onayade OA, Adebajo AC (2000) Composition of the leaf volatile oil of Murraya koenigii growing in Nigeria. J Herbs Spices Med Plants 7(4):59-66
51. Ondo JP, Lekana-Douki JB, Bongui JB, Zang Edou ES, Zatra R, Toure-Ndouo FS, Elomri A, Lebibi J, Seguin E (2012) In vitro antiplasmodial activity and cytotoxicity of extracts and fractions of Vitex madiensis, medicinal plant of Gabon. Trop Med Int Health 17(3):316-321
52. Orwa JA, Ngeny L, Mwikwabe NM, Ondicho J, Jondiko IJ (2013) Antimalarial and safety evaluation of extracts from Toddalia asiatica (L) Lam. (Rutaceae). J Ethnopharmacol 145(2):587-590
53. Peter LT, Anatoli VK (1998) The current global malaria situation. Malaria: parasite biology, pathogenesis and protection. ASM Press, Washington, DC, pp 11-22
54. Peters W, Portus JH, Robinson BL (1975) The chemotherapy of rodent malaria. XXII. The value of drug-resistant strains of Plasmodium berghei in screening for blood schizontocidal activity. Ann Trop Med Parasitol 69:155-171
55. Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, McGready R, Ler Moo C, Al-Saai S, Dondorp AM, Lwin KM, Singhasivanon P, Day NPJ, White NJ, Anderson TJ C, Nosten F (2012) Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet 379:1960-1966
56. Raina VK, Lal RK, Tripathi S, Khan M, Syamasundar KV, Srivastava SK (2002) Essential oil composition of genetically diverse stocks of Murraya koenigii from India. Flav Fragr J 17:144-146
57. Ramalhete C, Lopes D, Mulhovo S, Molnar J, Rosario VE, Ferreira MU (2010) New antimalarials with a triterpenic scaffold from Momordica balsamina. Bioorganic Med Chem 18:5254-5260
58. Rana VS, Juyal JP, Rashmi Blazquez MA (2004) Chemical constituents of the volatile oil of Murraya koenigii leaves. Int J Aromather 14:23-25
59. Rao LJM, Ramalakshmi K, Borse BB, Raghavan B (2007) Antioxidant and radical scavenging carbazole alkaloids from the oleoresin of curry leaf (Murraya koenigii Spreng). Food Chem 100:742-747
60. Rukunga GM, Muregi FW, Tolo FM, Omar SA, Mwitari P, Muthaura CN, Omlin F, Lwande W, Hassanali A, Githure J, Iraqi FW, Mungai GM, Kraus W, Kofi-Tsekpo WM (2007) The antiplasmodial activity of spermine alkaloids isolated from Albizia gummifera. Fitoterapia 78(7-8):455-459
61. Sathaye S, Bagul Y, Gupta S, Kaur H, Redkar R (2011) Hepatoprotective effects of aqueous leaf extract and crude isolates of Murraya koenigii against in vitro ethanol induced hepatotoxicity model. Exp Toxicol Pathol 63:587-591
62. Severino VG, Cazal Cde M, Forim MR, da Silva MF, Rodrigues-Filho E, Fernandes JB, Vieira PC (2009) Isolation of secondary metabolites from Hortia oreadica (Rutaceae) leaves through high-speed countercurrent chromatography. J Chromatogr A 1216(19):4275-4281
63. Shakya A (2012) Antimalarial activity of Acacia nilotica plant on Plasmodium berghei in mice. IJGHC 1(2):145-150
64. Shuaibu MN, Wuyep PA, Yanagi T, Hirayama K, Tanaka T, Kouno I (2008) The use of microfluorometric method for activity-guided isolation of antiplasmodial compound from plant extracts. Parasitol Res 102(6):1119-1127
65. Silva LFRE, Pinto ACS, Pohlit AM, Quignard EL, Vieira PP, Tadei WP, Chaves FC, Samonek JF, Lima CA, Costa MR, Alecrim M, Andrade-Neto VF (2011) In vivo and in vitro antimalarial activity of 4-nerolidylcatechol. Phytother Res 25(8):1181-1188
66. Simonsen HT, Nordskjold JB, Smitt UW, Nyman U, Palpu P, Joshi P, Varughese G (2001) In vitro screening of Indian medicinal plants for antiplasmodial activity. J Ethnopharmacol 74(2):195-204
67. Singh G, Marimuthu P, de Heluani CS, Catalan CA (2006) Antioxidant and biocidal activities of Carum nigrum (seed) essential oil, oleoresin, and their selected components. J Agric Food Chem 54:174-181
68. Sivakumar R, Jebanesan A, Govindarajan M, Rajasekar P (2011) Larvicidal and repellent activity of tetradecanoic acid against Aedes aegypti (Linn.) and Culex quinquefasciatus (Say.) (Diptera: Culicidae). Asian Pac J Trop Med 4(9):706-710
69. Smilkstein M, Sriwilaijaroen N, Kelly JX, Wilairat P, Riscoe M (2004) Simple and inexpensive fluorescence-based technique for high throughput antimalarial drug screening. Antimicrob Agents Chemother 48:1803-1806
70. Son IH, Chung IM, Lee SJ, Moon HI (2007) Antiplasmodial activity of novel stilbene derivatives isolated from Parthenocissus tricuspidata from South Korea. Parasitol Res 101(1):237-241
71. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193:673-675
72. Traore M, Diallo A, Nikiema JB, Tinto H, Dakuyo ZP, Ouedraogo JB, Guissou IP, Guiguemde TR (2008) In vitro and in vivo antiplasmodial activity of 'saye', an herbal remedy used in Burkina Faso traditional medicine. Phytother Res 22(4):550-551
73. Tundis R, Loizzo MR, Bonesi M, Menichini F, Dodaro D, Passalacqua NG, Statti G, Menichini F (2009) In vitro cytotoxic effects of Senecio stabianus Lacaita (Asteraceae) on human cancer cell lines. Nat Prod Res 23(18):1707-1718
74. Walde SG, Jyothirmayi T, Rao PGP, Srinivas P (2006) Flavour volatiles of flowers and stalks of Murraya koenigii L. Flav Fragr J 21:581-584
75. WHO (World Health Organization) (2012) World malaria report. World Global Malaria Program. http://www.who.int/malaria/publications/world-malaria-report- 2012/wmr2012-full-report.pdf
76. Willcox M, Bodeker R, Rasoanaivo P (2004) Traditional herbal medicines for modern times. Traditional medicinal plants and malaria. CRC, Boca Raton, p 431
77. Zhang WP, Ruan WB, Deng YY, Gao YB (2012) Potential antagonistic effects of nine natural fatty acids against Meloidogyne incognita. J Agric Food Chem 60(46):11631-11637
78. Zofou D, Kengne AB, Tene M, Ngemenya MN, Tane P, Titanji VP (2011) In vitro antiplasmodial activity and cytotoxicity of crude extracts and compounds from the stem bark of Kigelia africana (Lam.) Benth (Bignoniaceae). Parasitol Res 108(6):1383-1390
79. Zofou D, Tene M, Tane P, Titanji VP (2012) Antimalarial drug interactions of compounds isolated from Kigelia africana (Bignoniaceae) and their synergism with artemether, against the multidrug-resistant W2mef Plasmodium falciparum strain. Parasitol Res 110(2):539-544