CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES ›› 2018, Vol. 36 ›› Issue (6): 636-642.
• Orginal Article • Previous Articles Next Articles
Yun-shan MOU, Lu-jie LI, Yin-juan WU, Xue-rong LI*()
Received:
2018-04-25
Online:
2018-12-30
Published:
2019-01-08
Contact:
Xue-rong LI
E-mail:xuerong2@mail.sysu.edu.cn
Supported by:
CLC Number:
Yun-shan MOU, Lu-jie LI, Yin-juan WU, Xue-rong LI. Exploration of molecular mechanisms of artemisinin resistance in malaria parasites[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2018, 36(6): 636-642.
[1] | World Health Organization.World malaria report 2017[R]. Geneva: WHO, 2017. |
[2] | Udomsangpetch R, Pipitaporn B, Krishna S, et al. Antimalarial drugs reduce cytoadherence and rosetting Plasmodium falciparum[J]. J Infect Dis, 1996, 173(3): 691-698. |
[3] | ter Kuile F, White NJ, Holloway P, et al. Plasmodium falciparum: in vitro studies of the pharmacodynamic properties of drugs used for the treatment of severe malaria[J]. Exp Parasitol, 1993, 76(1): 85-95. |
[4] | Haldar K, Bhattacharjee S, Safeukui I.Drug resistance in Plasmodium[J]. Nat Rev Microbiol, 2018, 16(3): 156-170. |
[5] | Enserink M.Malaria’s drug miracle in danger[J]. Science, 2010, 328(5980): 844-846. |
[6] | Bhattarai A, Ali AS, Kachur SP, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar[J]. PLoS Med, 2007, 4(11): e309. |
[7] | Dondorp AM, Nosten F, Yi P, et al. Artemisinin resistance in Plasmodium falciparum malaria[J]. N Engl J Med, 2009, 361(5): 455-467. |
[8] | Amaratunga C, Sreng S, Suon S, et al. Artemisinin-resistant Plasmodium falciparum in Pursat province, western Cambodia: a parasite clearance rate study[J]. Lancet Infect Dis, 2012, 12(11): 851-858. |
[9] | Phyo AP, Nkhoma S, Stepniewska K, et al. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study[J]. Lancet, 2012, 379(9830): 1960-1966. |
[10] | Tun KM, Imwong M, Lwin KM, et al. Spread of artemisinin-resistant Plasmodium falciparum in Myanmar: a cross-sectional survey of the K13 molecular marker[J]. Lancet Infect Dis, 2015, 15(4): 415-421. |
[11] | Imwong M, Jindakhad T, Kunasol C, et al. An outbreak of artemisinin resistant falciparum malaria in Eastern Thailand[J]. Sci Reps, 2015, 5: 17412. |
[12] | Lu F, Culleton R, Zhang M, et al. Emergence of indigenous artemisinin-resistant Plasmodium falciparum in Africa[J]. N Engl J Med, 2017, 376(10): 991-993. |
[13] | Dhingra V, Vishweshwar Rao K, Lakshmi Narasu M.Current status of artemisinin and its derivatives as antimalarial drugs[J]. Life Sci, 2000, 66(4): 279-300. |
[14] | Umar RA, Hassan SW, Ladan MJ, et al. The association of K76T mutation in Pfcrt gene and chloroquine treatment failure in uncomplicated Plasmodium falciparum malaria in a cohort of Nigerian children[J]. J Appl Sci, 2007, 7(23): 3696-3704. |
[15] | Nsobya SL, Dokomajilar C, Joloba M, et al. Resistance-mediating Plasmodium falciparum Pfcrt and Pfmdr1 alleles after treatment with artesunate-amodiaquine in Uganda[J]. Antimicrob Agents Chemother, 2007, 51(8): 3023-3025. |
[16] | Holmgren G, Hamrin J, Svärd J, et al. Selection of Pfmdr1 mutations after amodiaquine monotherapy and amodiaquine plus artemisinin combination therapy in East Africa[J]. Infect Genet Evol, 2007, 7(5): 562-569. |
[17] | Henriques G, Hallett RL, Beshir KB, et al. Directional selection at the Pfmdr1, Pfcrt, Pfubp1, and Pfap2mu loci of Plasmodium falciparum in Kenyan children treated with ACT[J]. J Infect Dis, 2014, 210(12): 2001-2008. |
[18] | Price RN, Cassar C, Brockman A, et al. The Pfmdr1 gene is associated with a multidrug-resistant phenotype in Plasmodium falciparum from the western border of Thailand[J]. Antimicrob Agents Chemother, 1999, 43(12): 2943-2949. |
[19] | Chavchich M, Gerena L, Peters J, et al. Role of Pfmdr1 amplification and expression in induction of resistance to artemisinin derivatives in Plasmodium falciparum[J]. Antimicrob Agents Chemother, 2010, 54(6): 2455-2464. |
[20] | Price RN, Uhlemann AC, Brockman A, et al. Mefloquine resistance in Plasmodium falciparum and increased Pfmdr1 gene copy number[J]. Lancet, 2004, 364(9432): 438-447. |
[21] | Ibraheem ZO, Abd Majid R, Noor SM, et al. Role of different Pfcrt and Pfmdr-1 mutations in conferring resistance to antimalaria drugs in Plasmodium falciparum[J]. Malar Res Treat, 2014, 2014: 950424. |
[22] | Njokah MJ,Kang'ethe JN, Kinyua J, et al. In vitro selection of Plasmodium falciparum Pfcrt and Pfmdr1 variants by artemisinin[J]. Malar J, 2016, 15(1): 381. |
[23] | Sanchez CP, Mayer S, Nurhasanah A, et al. Genetic linkage analyses redefine the roles of PfCRT and PfMDR1 in drug accumulation and susceptibility in Plasmodium falciparum[J]. Mol Microbiol, 2011, 82(4): 865-878. |
[24] | Eckstein-Ludwig U, Webb RJ, Van Goethem ID, et al. Artemisinins target the SERCA of Plasmodium falciparum[J]. Nature, 2003, 424(6951): 957-961. |
[25] | Toyoshima C, Nomura H.Structural changes in the calcium pump accompanying the dissociation of calcium[J]. Nature, 2002, 418(6898): 605-611. |
[26] | N N, C GPD, Chakraborty C, et al. Mechanism of artemisinin resistance for malaria PfATP6 L263 mutations and discovering potential antimalarials: an integrated computational approach[J]. Scientific Reports, 2016, 6: 30106. |
[27] | Uhlemann AC, Cameron A, Eckstein-Ludwig U, et al. A single amino acid residue can determine the sensitivity of SERCAs to artemisinins[J]. Nat Struct Mol Biol, 2005, 12(7): 628-629. |
[28] | Jambou R, Martinelli A, Pinto J, et al. Geographic structuring of the Plasmodium falciparum sarco(endo) plasmic reticulum Ca2+ ATPase (PfSERCA) gene diversity[J]. PLoS One, 2010, 5(2): e9424. |
[29] | Cui L, Wang Z, Jiang H, et al. Lack of association of the S769N mutation in Plasmodium falciparum SERCA (PfATP6) with resistance to artemisinins[J]. Antimicrob Agents Chemother, 2012, 56(5): 2546-2552. |
[30] | Ariey F, Witkowski B, Amaratunga C, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria[J]. Nature, 2013, 505(7481): 50-55. |
[31] | Straimer J, Gnädig NF, Witkowski B, et al. Drug resistance. K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates[J]. Science, 2015, 347(6220): 428-431. |
[32] | World Health Organization.Guidelines for the Treatment of Malaria[M]. 3rd ed. Gevena: WHO, 2015. |
[33] | Itoh K, Wakabayashi N, Katoh Y, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain[J]. Genes Dev, 1999, 13(1): 76-86. |
[34] | Zhang DD, Hannink M.Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress[J]. Mol Cell Biol, 2003, 23(22): 8137-8151. |
[35] | Tilley L, Straimer J, Gnadig NF, et al. Artemisinin action and resistance in Plasmodium falciparum[J]. Trends Parasitol, 2016, 32(9): 682-696. |
[36] | Efferth T, Marschall M, Wang X, et al. Antiviral activity of artesunate towards wild-type, recombinant, and ganciclovir-resistant human cytomegaloviruses[J]. J Mol Med, 2002, 80(4): 233-242. |
[37] | Cheng C, Ho WE, Goh FY, et al. Anti-malarial drug artesunate attenuates experimental allergic asthma via inhibition of the phosphoinositide 3-kinase/Akt pathway[J]. PLoS One, 2011, 6(6): e20932. |
[38] | Bhattacharjee S, Stahelin RV, Speicher KD, et al. Endoplasmic reticulum PI(3)P lipid binding targets malaria proteins to the host cell[J]. Cell, 2012, 148(1/2): 201-212. |
[39] | Mbengue A, Bhattacharjee S, Pandharkar T, et al. A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria[J]. Nature, 2015, 520(7549): 683-687. |
[40] | Müller S.Role and regulation of glutathione metabolism in Plasmodium falciparum[J]. Molecules, 2015, 20(6): 10511-10534. |
[41] | Ittarat W, Sreepian A, Srisarin A, et al. Effect of dihydroartemisinin on the antioxidant capacity of P. falciparum-infected erythrocytes[J]. Southeast Asian J Trop Med Public Health, 2003, 34(4): 744-750. |
[42] | Phompradit P, Chaijaroenkul W, Na-Bangchang K.Cellular mechanisms of action and resistance of Plasmodium falciparum to artemisinin[J]. Parasitol Res, 2017, 116(12): 3331-3339. |
[43] | Fairhurst RM, Dondorp AM.Artemisinin-resistant Plasmodium falciparum malaria[J]. Microbiol Spectr, 2016, 4(3): EI10-0013-2016. |
[44] | Chandra R, Tripathi LM, Saxena JK, et al. Implication of intracellular glutathione and its related enzymes on resistance of malaria parasites to the antimalarial drug arteether[J]. Parasitol Int, 2011, 60(1): 97-100. |
[45] | Siddiqui G, Srivastava A, Russell AS, et al. Multi-omics based identification of specific biochemical changes associated with PfKelch13-mutant artemisinin-resistant Plasmodium falciparum[J]. J Infect Dis, 2017, 215(9): 1435-1444. |
[46] | Witkowski B, Lelièvre J, Nicolau-Travers ML, et al. Evidence for the contribution of the hemozoin synthesis pathway of the murine Plasmodium yoelii to the resistance to artemisinin-related drugs[J]. PLoS One, 2012, 7(3): e32620. |
[47] | 姚美雪, 王恒. 疟色素在疟原虫检测方面的应用研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2014, 32(1): 68-71. |
[48] | Meshnick SR, Thomas A, Ranz A, et al. Artemisinin (qinghaosu): the role of intracellular hemin in its mechanism of antimalarial action[J]. Mol Biochem Parasitol, 1991, 49(2): 181-189. |
[49] | Ron D, Walter P.Signal integration in the endoplasmic reticulum unfolded protein response[J]. Nat Rev Mol Cell Biol, 2007, 8(7): 519-529. |
[50] | Amm I, Sommer T, Wolf DH.Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system[J]. Biochim Biophys Acta, 2014, 1843(1): 182-196. |
[51] | Dogovski C, Xie SC, Burgio G, et al. Targeting the cell stress response of Plasmodium falciparum to overcome artemisinin resistance[J]. PLoS Biol, 2015, 13(4): e1002132. |
[52] | Mok S, Imwong M, Mackinnon MJ, et al. Artemisinin resistance in Plasmodium falciparum is associated with an altered temporal pattern of transcription[J]. BMC Genomics, 2011, 12: 391. |
[53] | Cazelles J, Robert A, Meunier B.Alkylation of heme by artemisinin, an antimalarial drug[J]. Comptes Rendus de l′Académie des Sciences-Series IIC-Chemistry, 2001, 4(2): 85-89. |
[54] | Haynes RK, Monti D, Taramelli D, et al. Artemisinin antimalarials do not inhibit hemozoin formation[J]. Antimicrob Agents Chemother, 2003, 47(3): 1175. |
[55] | Cazelles J, Camuzat-Dedenis B, Provot O, et al.ChemInform abstract: alkylating properties of synthetic trioxanes related to artemisinin[J]. ChemInform, 2010, 31(33): 1265-1270. |
[56] | Loup C, Lelièvre J, Benoit-Vical F, et al. Trioxaquines and heme-artemisinin adducts inhibit the in vitro formation of hemozoin better than chloroquine[J]. Antimicrob Agents Chemother, 2007, 51(10): 3768-3770. |
[57] | Karmodiya K, Pradhan S J, Joshi B, et al. A comprehensive epigenome map of Plasmodium falciparum reveals unique mechanisms of transcriptional regulation and identifies H3K36me2 as a global mark of gene suppression[J]. Epigenet Chromatin, 2015, 8(1): 32-49. |
[58] | Ay F, Bunnik EM, Varoquaux N, et al. Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression[J]. Genome Res, 2014, 24(6): 974-988. |
[59] | Ponts N, Fu L, Harris E, et al. Genome-wide mapping of DNA methylation in the human malaria parasite Plasmodium falciparum[J]. Cell Host Microbe, 2013, 14(6): 696-706. |
[60] | Ginsburg H, Kutner S, Krugliak M, et al. Characterization of permeation pathways appearing in the host membrane of Plasmodium falciparum infected red blood cells[J]. Mol Biochem Parasitol, 1985, 14(3): 313-322. |
[61] | Comeaux CA, Coleman BI, Bei AK, et al. Functional analysis of epigenetic regulation of tandem RhopH1/clag genes reveals a role in Plasmodium falciparum growth[J]. Mol Microbiol, 2011, 80(2): 378-390. |
[62] | Mohan R.Matrix metalloproteinase gelatinase B (MMP-9) coordinates and effects epithelial regeneration[J]. J Biol Chem, 2002, 277(3): 2065-2072. |
[63] | Mira-Martínez S, Rovira-Graells N, Crowley VM, et al. Epigenetic switches in clag3 genes mediate blasticidin S resistance in malaria parasites[J]. Cell Microbiol, 2013, 15(11): 1913-1923. |
[64] | Basore K, Cheng Y, Kushwaha AK, et al. How do antimalarial drugs reach their intracellular targets[J]. Front Pharmacol, 2015, 6: 91. |
[65] | 田一妮, 叶润, 潘卫庆, 等. 恶性疟原虫药物抗性相关基因筛选与鉴定方法[J]. 中国寄生虫学与寄生虫病杂志, 2017, 35(5): 495-498. |
[66] | Wang Z, Cabrera M, Yang J, et al. Genome-wide association analysis identifies genetic loci associated with resistance to multiple antimalarials in Plasmodium falciparum from China-Myanmar border[J]. Sci Rep, 2016, 6:33891. |
[67] | Mohanty S.Guidelines for the treatment of malaria[M]. Geneva: World Health Organization, 2006. |
[68] | 张丽, 丰俊, 张少森, 等. 2017年全国消除疟疾进展及疫情特征分析[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(3):201-209. |
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