ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Bailly E, Jambou R, Savel J, Jaureguiberry G, 1992. Plasmodium falciparum: differential sensitivity in vitro to E-64 (cysteine protease inhibitor) and pepstatin A (aspartyl protease inhibitor). J Protozool 39: 593– 599.
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Inhibitory Effects of Pepstatin A and Mefloquine on the Growth of Babesia Parasites
Tserendorj Munkhjargal
Tserendorj Munkhjargal
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Mahmoud AbouLaila
Mahmoud AbouLaila
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Mohamad Alaa Terkawi
Mohamad Alaa Terkawi
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Thillaiampalam Sivakumar
Thillaiampalam Sivakumar
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Madoka Ichikawa
Madoka Ichikawa
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Batdorj Davaasuren
Batdorj Davaasuren
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Tserendorj Nyamjargal
Tserendorj Nyamjargal
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Naoaki Yokoyama
Naoaki Yokoyama
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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Ikuo Igarashi
Ikuo Igarashi
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan; Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt; Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan, Ulaanbaatar, Mongolia
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We evaluated the inhibitory effects of pepstatin A and mefloquine on the in vitro and in vivo growths of Babesia parasites. The in vitro growth of Babesia bovis, B. bigemina, B. caballi, and B. equi was significantly inhibited (P < 0.05) by micromolar concentrations of pepstatin A (50% inhibitory concentrations = 38.5, 36.5, 17.6, and 18.1 μM, respectively) and mefloquine (50% inhibitory concentrations = 59.7, 56.7, 20.7, and 4 μM, respectively). Furthermore, both reagents either alone at a concentration of 5 mg/kg or in combinations (2.5/2.5 and 5/5 mg/kg) for 10 days significantly inhibited the in vivo growth of B. microti in mice. Mefloquine treatment was highly effective and the combination treatments were less effective than other treatments. Therefore, mefloquine may antagonize the actions of pepstatin A against babesiosis and aspartic proteases may play an important role in the asexual growth cycle of Babesia parasites.
Author Notes
Financial support: This study was supported by Grants-in-Aid for Scientific Research from the Japanese Society for the Promotion of Science, the Global Center of Excellence Program, Ministry of Education, Culture, Sports, Science, and Technology, Japan.
Authors' addresses: Tserendorj Munkhjargal, Mahmoud AbouLaila, Mohamad Alaa Terkawi, Thillaiampalam Sivakumar, Madoka Ichikawa, Batdorj Davaasuren, Tserendorj Nyamjargal, Naoaki Yokoyama, and Ikuo Igarashi, National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan, E-mails: muugii_f@yahoo.com, hethet2004@yahoo.com, alaaterkawi@hotmail.com, sivavets@gmail.com, ichikawa@obihiro.ac.jp, davlag_mgl@yahoo.com, nyama18@yahoo.com, yokoyama@obihiro.ac.jp, and igarcpmi@obihiro.ac.jp. Mahmoud AbouLaila, Department of Parasitology, Faculty of Veterinary Medicine, Minoufiya University, Sadat City, Minoufiya, Egypt, E-mail: hethet2004@yahoo.com. Batdorj Davaasuren, Laboratory of Molecular Genetic, Institute of Veterinary Medicine, Zaisan 210153, Ulaanbaatar, Mongolia, E-mails: davlag_mgl@yahoo.com.
Reprint requests: Ikuo Igarashi, National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan, E-mail: igarcpmi@obihiro.ac.jp.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Kuttler KL, 1988. World-wide impact of babesiosis. Ristic M, ed. Babesiosis of Domestic Animals and Man. Boca Raton, FL: CRC Press, 1– 22.
-
2.
Wright IG, Goodger BV, 1988. Pathogenesis of babesiosis. Ristic M, ed. Babesiosis of Domestic Animals and Man. Boca Raton, FL: CRC Press, 99– 118.
-
3.
Homer MJ, Aguilar-Delfin I, Telford III Sr., Krause PJ, Persing DH, 2000. Babesiosis. Clin Microbiol Rev 13: 451– 469.
-
4.
Kjemtrup AM, Conrad PA, 2000. Human babesiosis: an emerging tick-borne disease. Int J Parasitol 30: 1323– 1337.
-
5.
Vial HJ, Gorenflot A, 2006. Chemotherapy against babesiosis. Vet Parasitol 138: 147– 160.
-
6.
Bork S, Yokoyama N, Matsuo T, Claveria FG, Fujisaki K, Igarashi I, 2003a. Growth inhibitory effect of triclosan on equine and bovine Babesia parasites. Am J Trop Med Hyg 68: 334– 340.
-
7.
Nagai A, Yokoyama N, Matsuo T, Bork S, Hirata H, Xuan X, 2003. Growth-inhibitory effects of artesunate, pyrimethamine, and pamaquine against Babesia equi and Babesia caballi in in vitro cultures. Antimicrob Agents Chemother 47: 800– 803.
-
8.
Bork S, Yokoyama N, Ikehara Y, Kumar S, Sugimoto C, Igarashi I, 2004. Growth-inhibitory effect of heparin on Babesia parasites. Antimicrob Agents Chemother 48: 236– 241.
-
9.
Bork S, Das S, Okubo K, Yokoyama N, Igarashi I, 2006. Effect of protein kinase inhibitors on the in vitro growth of Babesia bovis. Parasitology 132: 775– 779.
-
10.
Okubo K, Yokoyama N, Govind Y, Alhassan A, Igarashi I, 2007. Babesia bovis: effects of cysteine protease inhibitors on in vitro growth. Exp Parasitol 117: 214– 217.
-
11.
Goldberg DE, Slater AFG, Beavis R, Chait B, Cerami A, Henderson GB, 1991. Hemoglobin degradation in the human malaria pathogen Plasmodium falciparum: a catabolic pathway initiated by a specific aspartic protease. JEM 173: 961– 969.
-
12.
Laurent F, Bourdieu C, Kaga M, Chilmonczyk S, Zgrzebski G, Yvore P, Pery P, 1993. Cloning and characterization of an Eimeria acervulina sporozoite gene homologous to aspartyl proteinases. Mol Biochem Parasitol 62: 303– 312.
-
13.
Jean L, Grosclaude J, Labbe M, Tomley F, Pery P, 2000. Differential localization of an Eimeria tenella aspartyl proteinase during the infection process. Int J Parasitol 30: 1099– 1107.
-
14.
Pinho R, Beltramini L, Alves C, De-Simone S, 2009. Trypanosoma cruzi: isolation and characterization of aspartyl proteases. Exp Parasitol 122: 128– 133.
-
15.
Francis SE, Gluzman IY, Oksman A, Knickerbocker A, Mueller R, Bryant ML, Sherman DR, Russell DG, Goldberg DE, 1994. Molecular characterization and inhibition of a Plasmodium falciparum aspartic hemoglobinase. EMBO J 13: 306– 317.
-
16.
Silva AM, Lee AY, Gulnik SV, Majer P, Collins J, Bhat TN, 1996. Structure and inhibition of plasmepsin II, a hemoglobin-degrading enzyme from Plasmodium falciparum. Proc Natl Acad Sci USA 93: 10034– 10039.
-
17.
Moon RP, Tyas L, Certa U, Rupp K, Bur D, Jacquet C, Matile H, Loetscher H, Grueninger-Leitch F, Kay J, Dunn BM, Berry C, Ridley RG, 1997. Expression and characterisation of plasmepsin I from Plasmodium falciparum. Eur J Biochem 244: 552– 560.
-
18.
Banerjee R, Liu J, Beatty W, Pelosof L, Klemba M, Goldberg DE, 2002. Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Proc Natl Acad Sci USA 99: 990– 995.
-
19.
Bailly E, Jambou R, Savel J, Jaureguiberry G, 1992. Plasmodium falciparum: differential sensitivity in vitro to E-64 (cysteine protease inhibitor) and pepstatin A (aspartyl protease inhibitor). J Protozool 39: 593– 599.
-
20.
Semenov A, Olson JE, Rosenthal PJ, 1998. Antimalarial synergy of cysteine and aspartic protease inhibitors. Antimicrob Agents Chemother 42: 2254– 2258.
-
21.
Sharma A, Eapen A, Subbararao SK, 2005. Purification and characterization of a hemoglobin degrading aspartic protease from the malarial parasite Plasmodium vivax. J Biochem 138: 71– 78.
-
22.
Palmer KJ, Holliday SM, Brogden RN, 1993. Mefloquine. A review of its antimalarial activity, pharmacokinetic properties and therapeutic efficacy. Drugs 45: 430– 475.
-
23.
Mockenhaupt FP, 1995. Mefloquine resistance in Plasmodium falciparum. Parasitol Today 11: 248– 253.
-
24.
Schlagenhauf P, 1999. Mefloquine for malaria chemoprophylaxis 1992–1998: a review. J Travel Med 6: 122– 133.
-
25.
Nevin RL, 2009. Epileptogenic potential of mefloquine chemoprophylaxis: a pathogenic hypothesis. Malar J 8: 188.
-
26.
Dorn A, Vippagunta SR, Matile H, Jaquet C, Vennerstrom JL, Ridley RG, 1998. An assessment of drug-haematin binding as a mechanism for inhibition of haematin polymerisation by quinoline antimalarials. Biochem Pharmacol 55: 727– 736.
-
27.
Mungthin M, Bray PG, Ridley RG, Ward SA, 1998. Central role of hemoglobin degradation in mechanisms of action of 4-aminoquinolines, quinoline methanols, and phenanthrene methanols. Antimicrob Agents Chemother 42: 2973– 2977.
-
28.
Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, 2007. Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 3: 1401– 1413.
-
29.
AbouLaila M, Nakamura K, Govind Y, Yokoyama N, Igarashi I, 2010a. Evaluation of the in vitro growth-inhibitory effect of epoxomicin on Babesia parasites. Vet Parasitol 167: 19– 27.
-
30.
Zweygarth E, Just MC, de Waal DT, 1995. Continuous in vitro cultivation of erythrocytic stages of Babesia equi. Parasitol Res 81: 355– 358.
-
31.
Erp EE, Smith RD, Ristic M, Osorno BM, 1980. Optimization of the suspension culture method for in vitro cultivation of Babesia bovis. Am J Vet Res 41: 2059– 2062.
-
32.
AbouLaila M, Munkhjargal T, Sivakumar T, Ueno A, Nakano Y, Yokoyama M, Yoshinari T, Nagano D, Katayama K, El-Bahy N, Yokoyama N, Igarashi I, 2012. Apicoplast-targeting antibacterials inhibit the growth of Babesia parasites. Antimicrob Agents Chemother 56: 3196– 3206.
-
33.
Bork S, Yokoyama N, Matsuo T, Claveria FG, Fujisaki K, Igarashi I, 2003c. Clotrimazole, ketoconazole, and clodinafop-propargyl inhibit the in vitro growth of Babesia bigemina and Babesia bovis (Phylum Apicomplexa). Parasitology 127: 311– 315.
-
34.
Rogers WO, Sem R, Tero T, Chim P, Lim P, Muth S, Socheat D, Ariey F, Wongsrichanalai C, 2009. Failure of artesunate-mefloquine combination therapy for uncomplicated Plasmodium falciparum malaria in southern Cambodia. Malar J 8: 10. doi:10.1186/1475-2875-8-10.
-
35.
Wurtz N, Briolant S, Gil M, Parquet V, Henry M, Baret E, Amalvict R, Almeras L, Rogier C, Pradines B, 2010. Synergy of mefloquine activity with atorvastatin, but not chloroquine and monodesethylamodiaquine, and association with the pfmdr1 gene. J Antimicrob Chemother 65: 1387– 1394.
-
36.
Lee HS, Go ML, 1996. Effects of mefloquine on Ca2+ uptake and release by dog brain microsomes. Arch Int Pharmacodyn Ther 331: 221– 231.
-
37.
Takabatake N, Hashiba S, Bork S, Okamura M, Yokoyama N, Igarashi I, 2004. Fucoidan inhibits the in vitro growth of Babesia bovis. J Protozool Res 14: 55– 60.
-
38.
Igarashi I, Njonge F, Kaneko Y, Nakamura Y, 1998. Babesia bigemina: in vitro and in vivo effects of curdlan sulfate on the growth of parasites. Exp Parasitol 90: 290– 293.
-
39.
Munkhjargal T, Aboulaila M, Sivakumar T, Yokoyama N, Igarashi I, 2009. Inhibitory effect of apicidin on in vitro and in vivo growth of Babesia parasites. J Protozool Res 19: 42– 49.
-
40.
Bork S, Yokoyama N, Matsuo T, Claveria FG, Fujisaki K, Igarashi I, 2003b. Clotrimazole, ketoconazole, and clodinafop-propargyl inhibit the in vitro growth of Babesia bigemina and Babesia bovis (Phylum Apicomplexa). Parasitology 127: 311– 315.
-
41.
AbouLaila M, Yokoyama N, Igarashi I, 2010b. Inhibitory effect of (-)-Epigallocatechin-3-gallate from green tea on the growth of Babesia parasites. Parasitology 137: 7858– 7791.
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