Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate

Babesiosis is a disease brought on by intraerythrocytic parasites of the genus Babesia. Current chemotherapies are accompanied by side effects and parasite relapse. Therefore, it is crucial to develop highly effective drugs against Babesia. Cipargamin (CIP) has shown inhibition against apicomplexan...

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Main Authors: Hang Li, Shengwei Ji, Nanang R Ariefta, Eloiza May S Galon, Shimaa AES El-Sayed, Thom Do, Lijun Jia, Miako Sakaguchi, Masahito Asada, Yoshifumi Nishikawa, Xin Qin, Mingming Liu, Xuenan Xuan
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Language:English
Published: eLife Sciences Publications Ltd 2025-06-01
Series:eLife
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Online Access:https://elifesciences.org/articles/101128
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author Hang Li
Shengwei Ji
Nanang R Ariefta
Eloiza May S Galon
Shimaa AES El-Sayed
Thom Do
Lijun Jia
Miako Sakaguchi
Masahito Asada
Yoshifumi Nishikawa
Xin Qin
Mingming Liu
Xuenan Xuan
author_facet Hang Li
Shengwei Ji
Nanang R Ariefta
Eloiza May S Galon
Shimaa AES El-Sayed
Thom Do
Lijun Jia
Miako Sakaguchi
Masahito Asada
Yoshifumi Nishikawa
Xin Qin
Mingming Liu
Xuenan Xuan
author_sort Hang Li
collection DOAJ
description Babesiosis is a disease brought on by intraerythrocytic parasites of the genus Babesia. Current chemotherapies are accompanied by side effects and parasite relapse. Therefore, it is crucial to develop highly effective drugs against Babesia. Cipargamin (CIP) has shown inhibition against apicomplexan parasites, mainly Plasmodium and Toxoplasma. This study evaluated the growth-inhibiting properties of CIP against Babesia spp. and investigated the mechanism of CIP on B. gibsoni. The half inhibitory concentration (IC50) values of CIP against the in vitro growth of B. bovis and B. gibsoni were 20.2 ± 1.4 and 69.4 ± 2.2 nM, respectively. CIP significantly inhibited the growth of B. microti and B. rodhaini in vivo. Resistance was conferred by L921V and L921I mutations in BgATP4, which reduced the sensitivity to CIP by 6.1- and 12.8-fold. The inhibitory potency of CIP against BgATP4-associated ATPase activity was moderately reduced in mutant strains, with a 1.3- and 2.4-fold decrease in BgATP4L921V and BgATP4L921I, respectively, compared to that of BgATP4WT. An in silico investigation revealed reductions in affinity for CIP binding to BgATP4L921V and BgATP4L921I compared to BgATP4WT. Resistant strains showed no significant cross-resistance to atovaquone or tafenoquine succinate (TQ), with less than a onefold change in IC50 values. Combining CIP with TQ effectively eliminated B. microti infection in SCID mice with no relapse, and parasite DNA was not detected by qPCR within 90 days post-infection. Our findings reveal the efficacy of CIP as an antibabesial agent, its limitations as a monotherapy due to resistance development, and the potential of combination therapy with TQ to overcome said resistance and achieve complete parasite clearance.
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spelling doaj-art-1d82b1bb17b448c588167909eb82d0aa2025-08-20T03:31:12ZengeLife Sciences Publications LtdeLife2050-084X2025-06-011310.7554/eLife.101128Efficacy and mechanism of action of cipargamin as an antibabesial drug candidateHang Li0https://orcid.org/0009-0008-6361-8955Shengwei Ji1https://orcid.org/0000-0001-7380-4809Nanang R Ariefta2https://orcid.org/0000-0002-3012-6005Eloiza May S Galon3https://orcid.org/0000-0003-2411-8401Shimaa AES El-Sayed4Thom Do5Lijun Jia6Miako Sakaguchi7Masahito Asada8https://orcid.org/0000-0003-0042-6856Yoshifumi Nishikawa9https://orcid.org/0000-0001-5005-6377Xin Qin10https://orcid.org/0000-0001-6448-5180Mingming Liu11https://orcid.org/0000-0002-5935-6736Xuenan Xuan12https://orcid.org/0000-0003-2780-110XNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, JapanNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, Japan; Department of Veterinary Medicine, Agriculture College of Yanbian University, Yanji, ChinaNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, JapanCollege of Veterinary Medicine and Biomedical Sciences, Cavite State University, Indang, PhilippinesNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, Japan; Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Mansoura University, Mansoura, EgyptNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, JapanDepartment of Veterinary Medicine, Agriculture College of Yanbian University, Yanji, ChinaCentral Laboratory, Institute of Tropical Medicine (NEKKEN), Nagasaki University, Nagasaki, JapanNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, JapanNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, JapanSchool of Basic Medicine, Hubei University of Arts and Science, Xiangyang, ChinaSchool of Basic Medicine, Hubei University of Arts and Science, Xiangyang, ChinaNational Research Center for Protozoan Diseases, Obihiro University of Agriculture Veterinary Medicine, Obihiro, Japan; Research Center for Asian Infectious Diseases, The University of Tokyo, Tokyo, JapanBabesiosis is a disease brought on by intraerythrocytic parasites of the genus Babesia. Current chemotherapies are accompanied by side effects and parasite relapse. Therefore, it is crucial to develop highly effective drugs against Babesia. Cipargamin (CIP) has shown inhibition against apicomplexan parasites, mainly Plasmodium and Toxoplasma. This study evaluated the growth-inhibiting properties of CIP against Babesia spp. and investigated the mechanism of CIP on B. gibsoni. The half inhibitory concentration (IC50) values of CIP against the in vitro growth of B. bovis and B. gibsoni were 20.2 ± 1.4 and 69.4 ± 2.2 nM, respectively. CIP significantly inhibited the growth of B. microti and B. rodhaini in vivo. Resistance was conferred by L921V and L921I mutations in BgATP4, which reduced the sensitivity to CIP by 6.1- and 12.8-fold. The inhibitory potency of CIP against BgATP4-associated ATPase activity was moderately reduced in mutant strains, with a 1.3- and 2.4-fold decrease in BgATP4L921V and BgATP4L921I, respectively, compared to that of BgATP4WT. An in silico investigation revealed reductions in affinity for CIP binding to BgATP4L921V and BgATP4L921I compared to BgATP4WT. Resistant strains showed no significant cross-resistance to atovaquone or tafenoquine succinate (TQ), with less than a onefold change in IC50 values. Combining CIP with TQ effectively eliminated B. microti infection in SCID mice with no relapse, and parasite DNA was not detected by qPCR within 90 days post-infection. Our findings reveal the efficacy of CIP as an antibabesial agent, its limitations as a monotherapy due to resistance development, and the potential of combination therapy with TQ to overcome said resistance and achieve complete parasite clearance.https://elifesciences.org/articles/101128Babesia spp.cipargamindrug resistance
spellingShingle Hang Li
Shengwei Ji
Nanang R Ariefta
Eloiza May S Galon
Shimaa AES El-Sayed
Thom Do
Lijun Jia
Miako Sakaguchi
Masahito Asada
Yoshifumi Nishikawa
Xin Qin
Mingming Liu
Xuenan Xuan
Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
eLife
Babesia spp.
cipargamin
drug resistance
title Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
title_full Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
title_fullStr Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
title_full_unstemmed Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
title_short Efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
title_sort efficacy and mechanism of action of cipargamin as an antibabesial drug candidate
topic Babesia spp.
cipargamin
drug resistance
url https://elifesciences.org/articles/101128
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