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Mosquito Larvicidal Activity of Pipernonaline, a Piperidine Alkaloid Derived from Long Pepper

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Mosquito Larvicidal Activity of Pipernonaline, a Piperidine Alkaloid Derived from Long Pepper Journal of the American Mosquito Control Association, 16(3):245-247, 200,O Copyright O 2000 by the American Mosquito Control Association, Inc. MOSQUITO LARVICIDAL ACTIVITY OF PIPERNONALINE, A PIPERIDINE ALKALOID DERIVED FROM LONG PEPPER. PIPER LONGUM SUNG-EUN LEE Plant Protection Research Unit, WRRC, USDA-ARS, 800 Buchanan Street, Albany, CA 94710 ABSTRACT. A methanol extract of Piper longum fruit was found to be active against mosquito larvae of Culex pipiens pallens at l0 pglml after 24 h. A piperidine alkaloid, pipernonaline, was found to be responsible for this activity, with the 24-h rnedian lethal dose (LDr) value for this compound being 0.21 mg/liter. The LDro value of pipernonaline was not much higher than those for the 3 organophosphorous insecticides malathion, chlorpyrifos-methyl, and pirimiphos-methyl, used for comparative purpose in this study. Structural elucidation of pipernonaline was by means of mass spectrometry ('H and r3C nuclear magnetic resonance imaging). KEY WORDS Piper longum, pipernonaline, mosquito larvicidal activity, Culex pipiens INTRODUCTION perature and filtered (Toyo filter paper no. 2, Tokyo, Japan). The combined filtrate was concentrated in Mosquito-borne diseases such as malaria, filari- vacuo at 35'C to yield about 9.8Vo(on the basis of asis, dengue, yellow fever, and Japanese encepha- the weight of the dried fruit). The extract (20 g) litis contribute significantly to disease burden, was sequentially partitioned into hexane (3.8 g), death, poverty, and social debility in the world. chloroform (4.3 g, ethyl acetate(1.4 g, and water- Among these diseases, malaria continues to be a soluble (10.5 g) portions for subsequentbioassay major public health problem in most counhies of with 3rd instars of Cx. p. pallens. The organic sol- the tropical world. For example, the World Health vent portions were concentrated to dryness by ro- Organization (WHO) reported that 22OO million tatory evaporation at 35'C, and the water portion people were exposed to malarial infections in some was freeze-dried. The active hexane portion was 9O countries or areas and that malaria was also the chromatographed on a silica gel colufirr (Merck 70- cause of an estimated 1.4--2.6 million deaths world- 230 mesh, 300 g, 4.5 inner diameter X 60 cm; wide every year, with more than 907o of these Merck, Whitehouse Station, NJ) and successively deaths occurring in Africa alone (WHO 1992). eluted with hexane-ethyl acetate, ethyl acetate, and However, control of malarial and other mosquito- ethyl acetate-methanol.The active fractions eluted borne diseases is becoming increasingly difficult. with hexane-ethyl acetate (3:1) were chromato- The effectiveness ofvector control has declined be- graphed on a silica gel column and eluted with hex- cause of reduced effectiveness of insecticides ane-ethyl acetate(4:1). Column fractions were col- caused by emergence of resistance in mosquitoes lected and aralyzed by thin-layer chromatography against the currently used insecticides (Chandre et (TLC; hexane-ethyl acetate,3:1). Fractions with a al. 1998, Penilla et al. 1998). It is also important to similar TLC pattern were combined. For further recognize that only a limited number of pesticides separationof the mosquito larvicidal substances,a are available for use in public health. Therefore, an Waters Delta Prep 40O0 high-performance liquid effort to find alternatives for the currently used in- chromatography (Waters Co., Milford, MA) was secticides in relation to mosquito control may be used.The colurnn was 29 inner diameter X 300 mm needed. Bondapak Cl8 (Waters) using methanol:water (3: The use of botanical derivatives in the control of 7) at a flow rate of 7 mVmin and detection at 260 mosquito larvae may offer a more environmentally nm. Compound I (28 mg) was isolated. safe method of insect control than the use of syn- Structural determination of the active isolate was thetic chemicals. In this paper, I report isolation based on spectral analysis. 'H (400 MHz) and '3C procedures and structural determinations of a pi- nuclear magnetic resonance (NMR; l0O MHz) peridine alkaloid active against mosquito larvae of spectra were measured in dimethylsulfoxide-du at Culex pipiens pallens Coq. from the methanolic ex- room temperature on a Bruker AMX-400 (Bruker tract of the dried fruits of the long pepper, Piper Instrument [nc., Fremont, CA) with tetramethylsi- longum L. lane as an internal standard. Mass spectra were done on a JEOL JMS-DX3O specffometer (JEOL MATERIALS AI{D METHODS USA Inc., Fremont, CA). Extraction and isolation. Bioassay Dried fruits (2.5 kg) of P. longum, obtained from a traditional market in Seoul, were crushed and ex- Five hundred female mosquitoes, Cx. p. pallens tracted twice with methanol (10 liters) at room tem- (F-256 larvae were acquiredfrom Korean Food and 245 246 JounrlAr-or rm AupnrcAN Moseuno Corvrnol Assocrenon Vor. 16, No. 3 Table l. Regressionparametersformortalityresponseof 3rd-stage Culexpipienspallens Cog. larvaeexposedto pipernonaline and 3 organophosphorous insecticides: chlorpyrifos-methyl, pirimiphos-methyl, and malathion.r Compound LDro LDrt Slope Pipernonaline o.2r (0.17--0.28) 0.52 (0.48--0.57) 2.1 Chlorpyrifos-methyl 0.00037(0.00022-0.00058) 0.001l (0.00078-0.0015) 4.6 Malathion 0.016 (0-009-0.023) 0.078 (0.056{.096) 2.5 Pirimiphos-methyl 0.1I (0.09-{.14) 0.17 (0.15-o.18) 7.8 I Doses expressed in mg/liter; LD,o, median lethal dose; LD*959o lethal dose. Drug Administration, Seoul, Korea), were used in (4H, br m), 3.50 (4H, br m), 5.90 (lH, d, J : l5.O this study. All bioassays were done in an environ- Ha C,-H), 5.92 (2H, s, -OCH,O- ), 6.0I - 6.38 (2H, mentally controlled room maintained at 3O -r l"C m),6.73 (2H, br s, C5,.6,-H),6.80 (lH, dt, J : 15.0, and 80 + 5Vo relative humidity. Larval testing was 4.O H4 C3-H),6.88 (lH, s, Cr,-H). I3CNMR: Ta- done on 5 acetone serial dilutions of pipernonaline, ble 2. chlorpyrifos-methyl, malathion, and pirimiphos- The fruits of some Piperaceae plants have been methyl. One hundred milliliters of each test solu- known for their use as food flavoring agents and tion was placed into a Pyrex dish (lOO X 50 mm; also for containing insecticidal properties (Miyak- Fisher Scientific, Pittsburgh, PA) along with thirty ado et al. 1979, Su and Horvat 1981,Tlagi et al. 3rd instars. Each dilution, along with an untreated 1993). Among these components,unsaturated am- control group (acetone carrier and water), was rep- ides constitute a major group of secondary metab- licated 5 times. Mortality recorded at 24 h after olites. Dry black pepper,Piper nigrum L., which is treatrnent, median lethal dose (LDro), and 95Vo le- available from the supermarket, has been reported thal dose values were calculated by probit analysis to be toxic to houseflies(Musca domesticaL.), rice (Finney 1971). Control mortality was accounted for weevils (Sitophilus oryzae L.), and cowpea weevils by Abbou's formula (Abbou 1925). (Callosobruchus maculatus Fabr.; Su 1977, Scott and McKibben 1978, Su and Horvat 1981). Piper- ine is easily isolated from the fruit of the black RESULTS AND DISCUSSION pepper plant, although it is apparently inactive as During the initial experiments, we observed that a contact toxicant (Su and Horvat 1981). However, methanolic extract of P. longum fruits possessed several insecticidal amides, such as pipericide, mosquito larvicidal activity against Cx. p. pallens, (E,E) -N - (2-methylpropyl) -2,4 - decadienamide, and also only I mgAiter of hexane fraction had a (E,E, E)- 13-(1,3 -benzodioxol-5 -yl)-N-(2-methyl- strong larvicidal activity of IOOVomortality. Mod- propyl)-2,4,12-tridecatrienamide, and (E,E, E)-l 1- erate activity and little activity were produced from ( l, 3-benzodioxol-5 -yl)-N-(2-methylpropyl)- other organic solvent fractions. No activity was ob- 2.4.1 0-undecatrienamide. have been isolated from served in the water fraction. One active isolate from the pepper plant (Miyakado et al. 1979, Su and the hexane fraction showed potent larvicidal activ- Horvat 1981). ity, shown in Table 1, and it was characterizedby Pipernonalinehas been isolated from P. longum the spectral analyses as pipernonaline (Fig. l). (Tabunenget al. 1983), but its biological activity has not been determined. Herein, I report that this compound has a potent larvicidal Fipernonaline activity against 3rd-stagelarvae of Cx. p. pallent with 24-h LDso Pale yellow needles. UV I** EIOH: 364.2 nm. values of just 0.21 mg/liter (Table l). This LDro Found [M]* m/z 341.2336. EI-MS m./z (rel. int.): value of pipernonaline was 27-fold, 110-fold, and 341 (4s),273 (r8),228 (37),206 (61), r93 (2O), 245-fold stronger than those of obacunone, nomilin, 166(100), 153 (30), 131 (7s), 103 (75), 84 (4s). and limonin, respectively (Jayaprankashaet al. 'H NMR (E): 1.28-1.74(10H, br m), 2.W-2.36 1997). However, this LDro value of pipernonaline lu o. ( o 4' D::: 5' 4" Fig. 1. Structure of pipernonaline isolated from Piper longwnL. Spp,reN{sen2000 Moseurro LlnvrcrolL AcnvITy or PrprnNoNnLINe 247 Table 2. r3C Nuclear magnetic resonance (CDClr) data Chandre E, Darriet E, Darder M, Cuany A, Doannio JMC, of pipernonaline. Pasteur N, Guillet P. 1998. Pyrethroid resistance in Cu- quinquefosciatus from West Africa. Med Vet Ento- t3C Lex Pipernonaline mol 72:359-366. I 165.2 Finney DJ. 1971. Probit an4lysis Edition 3. London, Unit- 2 120.5 ed Kingdom: Cambridge University. J 145.2 Jayaprankasha GK, Singh PR, Pereira J, Sakariah KK. 32.2 1997. Limonoids from Citrus reticulata and their moult ) 27.9 inhibiting activity in mosquito Culex quinquefasciatus 6 28.9 larvae.
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