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Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Leishmaniasis: Omics Approaches to Understand its Biology from Molecule to Cell Level

Author(s): Indu Kumari, Dinesh Lakhanpal, Sandeep Swargam* and Anupam Nath Jha*

Volume 24, Issue 3, 2023

Published on: 01 March, 2023

Page: [229 - 239] Pages: 11

DOI: 10.2174/1389203724666230210123147

Price: $65

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Abstract

Leishmaniasis is the second deadliest vector-borne, neglected tropical zoonotic disease and is found in a variety of clinical forms based on genetic background. Its endemic type is present in tropical, sub-tropical and Mediterranean areas around the world which accounts for a lot of deaths every year. Currently, a variety of techniques are available for detection of leishmaniasis each technique having it's own pros and cons. The advancing next-generation sequencing (NGS) techniques are employed to find out novel diagnostic markers based on single nucleotide variants. A total of 274 NGS studies are available in European Nucleotide Archive (ENA) portal (https://www.ebi.ac.uk/ena/browser/home) that focused on wild-type and mutated Leishmania, differential gene expression, miRNA expression, and detection of aneuploidy mosaicism by omics approaches. These studies have provided insights into the population structure, virulence, and extensive structural variation, including known and suspected drug resistance loci, mosaic aneuploidy and hybrid formation under stressed conditions and inside the midgut of the sandfly. The complex interactions occurring within the parasite-host-vector triangle can be better understood by omics approaches. Further, advanced CRISPR technology allows researchers to delete and modify each gene individually to know the importance of genes in the virulence and survival of the disease-causing protozoa. In vitro generation of Leishmania hybrids are helping to understand the mechanism of disease progression in its different stages of infection. This review will give a comprehensive picture of the available omics data of various Leishmania spp. which helped to reveal the effect of climate change on the spread of its vector, the pathogen survival strategies, emerging antimicrobial resistance and its clinical importance.

Graphical Abstract

[1]
Malecela, M.N.; Ducker, C. A road map for neglected tropical diseases 2021–2030.Trans. R. Soc. Trop. Med. Hyg; Oxford University Press, 2021, pp. 121-123.
[2]
Das, N.K.; Ghosh, P.; Roy, P.; Chaudhuri, S.J. Epidemiology of post-kala-azar dermal leishmaniasis. Indian J. Dermatol., 2021, 66(1), 12-23.
[http://dx.doi.org/10.4103/ijd.IJD_651_20] [PMID: 33911289]
[3]
Stauch, A.; Duerr, H.P.; Dujardin, J.C.; Vanaerschot, M.; Sundar, S.; Eichner, M. Treatment of visceral leishmaniasis: Model-based analyses on the spread of antimony-resistant L. donovani in Bihar, India. PLoS Negl. Trop. Dis., 2012, 6(12), e1973.
[http://dx.doi.org/10.1371/journal.pntd.0001973] [PMID: 23285309]
[4]
Malaviya, P.; Picado, A.; Hasker, E.; Ostyn, B.; Kansal, S.; Singh, R.P.; Shankar, R.; Boelaert, M.; Sundar, S. Health & Demographic surveillance system profile: the Muzaffarpur-TMRC health and demographic surveillance system. Int. J. Epidemiol., 2014, 43(5), 1450-1457.
[http://dx.doi.org/10.1093/ije/dyu178] [PMID: 25186307]
[5]
Sundar, S.; Singh, A. Chemotherapeutics of visceral leishmaniasis: Present and future developments. Parasitology, 2018, 145(4), 481-489.
[http://dx.doi.org/10.1017/S0031182017002116] [PMID: 29215329]
[6]
Lata, S.; Kumar, G.; Ojha, V.P.; Dhiman, R.C. Detection of Leishmania donovani in wild-caught phlebotomine sand flies in endemic focus of leishmaniasis in Himachal Pradesh, India. J. Med. Entomol., 2022, 59(2), 719-724.
[http://dx.doi.org/10.1093/jme/tjab202] [PMID: 34865089]
[7]
Imamura, H.; Downing, T.; Van den Broeck, F.; Sanders, M.J.; Rijal, S.; Sundar, S.; Mannaert, A.; Vanaerschot, M.; Berg, M.; De Muylder, G.; Dumetz, F.; Cuypers, B.; Maes, I.; Domagalska, M.; Decuypere, S.; Rai, K.; Uranw, S.; Bhattarai, N.R.; Khanal, B.; Prajapati, V.K.; Sharma, S.; Stark, O.; Schönian, G.; De Koning, H.P.; Settimo, L.; Vanhollebeke, B.; Roy, S.; Ostyn, B.; Boelaert, M.; Maes, L.; Berriman, M.; Dujardin, J.C.; Cotton, J.A. Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent. eLife, 2016, 5, e12613.
[http://dx.doi.org/10.7554/eLife.12613] [PMID: 27003289]
[8]
Franssen, S.U.; Durrant, C.; Stark, O.; Moser, B.; Downing, T.; Imamura, H.; Dujardin, J.C.; Sanders, M.J.; Mauricio, I.; Miles, M.A.; Schnur, L.F.; Jaffe, C.L.; Nasereddin, A.; Schallig, H.; Yeo, M.; Bhattacharyya, T.; Alam, M.Z.; Berriman, M.; Wirth, T.; Schönian, G.; Cotton, J.A. Global genome diversity of the Leishmania donovani complex. eLife, 2020, 9, e51243.
[http://dx.doi.org/10.7554/eLife.51243] [PMID: 32209228]
[9]
Lypaczewski, P.; Matlashewski, G. Leishmania donovani hybridisation and introgression in nature: A comparative genomic investigation. Lancet Microbe, 2021, 2(6), e250-e258.
[http://dx.doi.org/10.1016/S2666-5247(21)00028-8] [PMID: 35544170]
[10]
Downing, T.; Imamura, H.; Decuypere, S.; Clark, T.G.; Coombs, G.H.; Cotton, J.A.; Hilley, J.D.; de Doncker, S.; Maes, I.; Mottram, J.C.; Quail, M.A.; Rijal, S.; Sanders, M.; Schönian, G.; Stark, O.; Sundar, S.; Vanaerschot, M.; Hertz-Fowler, C.; Dujardin, J.C.; Berriman, M. Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Res., 2011, 21(12), 2143-2156.
[http://dx.doi.org/10.1101/gr.123430.111] [PMID: 22038251]
[11]
Carnielli, J.B.T.; Crouch, K.; Forrester, S.; Silva, V.C.; Carvalho, S.F.G.; Damasceno, J.D.; Brown, E.; Dickens, N.J.; Costa, D.L.; Costa, C.H.N.; Dietze, R.; Jeffares, D.C.; Mottram, J.C. A Leishmania infantum genetic marker associated with miltefosine treatment failure for visceral leishmaniasis. EBioMedicine, 2018, 36, 83-91.
[http://dx.doi.org/10.1016/j.ebiom.2018.09.029] [PMID: 30268832]
[12]
Inbar, E.; Shaik, J.; Iantorno, S.A.; Romano, A.; Nzelu, C.O.; Owens, K.; Sanders, M.J.; Dobson, D.; Cotton, J.A.; Grigg, M.E.; Beverley, S.M.; Sacks, D. Whole genome sequencing of experimental hybrids supports meiosis-like sexual recombination in Leishmania. PLoS Genet., 2019, 15(5), e1008042.
[http://dx.doi.org/10.1371/journal.pgen.1008042] [PMID: 31091230]
[13]
Nolder, D.; Miles, M.A.; Llanos-Cuentas, A.; Davies, C.R.; Roncal, N. Multiple hybrid genotypes of Leishmania (viannia) in a focus of mucocutaneous Leishmaniasis. Am. J. Trop. Med. Hyg., 2007, 76(3), 573-578.
[http://dx.doi.org/10.4269/ajtmh.2007.76.573] [PMID: 17360886]
[14]
Ravel, C.; Cortes, S.; Pratlong, F.; Morio, F.; Dedet, J.P.; Campino, L. First report of genetic hybrids between two very divergent Leishmania species: Leishmania infantum and Leishmania major. Int. J. Parasitol., 2006, 36(13), 1383-1388.
[http://dx.doi.org/10.1016/j.ijpara.2006.06.019] [PMID: 16930606]
[15]
Cotton, J.A.; Durrant, C.; Franssen, S.U.; Gelanew, T.; Hailu, A.; Mateus, D.; Sanders, M.J.; Berriman, M.; Volf, P.; Miles, M.A.; Yeo, M. Genomic analysis of natural intra-specific hybrids among Ethiopian isolates of Leishmania donovani. PLoS Negl. Trop. Dis., 2020, 14(4), e0007143.
[http://dx.doi.org/10.1371/journal.pntd.0007143] [PMID: 32310945]
[16]
Requena, J.M.; Rastrojo, A.; Garde, E.; López, M.C.; Thomas, M.C.; Aguado, B. Genomic cartography and proposal of nomenclature for the repeated, interspersed elements of the Leishmania major SIDER2 family and identification of SIDER2-containing transcripts. Mol. Biochem. Parasitol., 2017, 212, 9-15.
[http://dx.doi.org/10.1016/j.molbiopara.2016.12.009] [PMID: 28034676]
[17]
Iourov, I.Y.; Vorsanova, S.G.; Soloviev, I.V.; Yurov, Y.B. Interphase FISH: Detection of intercellular genomic variations and somatic chromosomal mosaicism. In: Flouresence In situ Hybridization (FISH)-Application Guide; Liechr, T., Ed.; Springer Protocols Handbooks, Springer: Heidelberg, 2009; pp. 301-311.
[http://dx.doi.org/10.1007/978-3-540-70581-9_27]
[18]
Santi, A.M.M.; Murta, S.M.F. Impact of genetic diversity and genome plasticity of leishmania spp. in treatment and the search for novel chemotherapeutic targets. Front. Cell. Infect. Microbiol., 2022, 12, 826287.
[http://dx.doi.org/10.3389/fcimb.2022.826287] [PMID: 35141175]
[19]
Sterkers, Y.; Crobu, L.; Lachaud, L.; Pagès, M.; Bastien, P. Parasexuality and mosaic aneuploidy in Leishmania: Alternative genetics. Trends Parasitol., 2014, 30(9), 429-435.
[http://dx.doi.org/10.1016/j.pt.2014.07.002] [PMID: 25073852]
[20]
Rogers, M.B.; Hilley, J.D.; Dickens, N.J.; Wilkes, J.; Bates, P.A.; Depledge, D.P.; Harris, D.; Her, Y.; Herzyk, P.; Imamura, H.; Otto, T.D.; Sanders, M.; Seeger, K.; Dujardin, J.C.; Berriman, M.; Smith, D.F.; Hertz-Fowler, C.; Mottram, J.C. Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res., 2011, 21(12), 2129-2142.
[http://dx.doi.org/10.1101/gr.122945.111] [PMID: 22038252]
[21]
Laffitte, M.C.N.; Leprohon, P.; Papadopoulou, B.; Ouellette, M. Plasticity of the Leishmania genome leading to gene copy number variations and drug resistance. F1000 Res., 2016, 5, 2350.
[http://dx.doi.org/10.12688/f1000research.9218.1] [PMID: 27703673]
[22]
Sinha, R. C, M.M.; Raghwan; Das, S.; Das, S.; Shadab, M.; Chowdhury, R.; Tripathy, S.; Ali, N. Genome plasticity in cultured Leishmania donovani: Comparison of early and late passages. Front. Microbiol., 2018, 9, 1279.
[http://dx.doi.org/10.3389/fmicb.2018.01279] [PMID: 30018594]
[23]
Zhang, W.W.; Ramasamy, G.; McCall, L.I.; Haydock, A.; Ranasinghe, S.; Abeygunasekara, P.; Sirimanna, G.; Wickremasinghe, R.; Myler, P.; Matlashewski, G. Genetic analysis of Leishmania donovani tropism using a naturally attenuated cutaneous strain. PLoS Pathog., 2014, 10(7), e1004244.
[http://dx.doi.org/10.1371/journal.ppat.1004244] [PMID: 24992200]
[24]
Rastrojo, A.; Corvo, L.; Lombraña, R.; Solana, J.C.; Aguado, B.; Requena, J.M. Analysis by RNA-seq of transcriptomic changes elicited by heat shock in Leishmania major. Sci. Rep., 2019, 9(1), 6919.
[http://dx.doi.org/10.1038/s41598-019-43354-9] [PMID: 31061406]
[25]
Ty, M.C.; Loke, P.; Alberola, J.; Rodriguez, A.; Rodriguez-Cortes, A. Immuno-metabolic profile of human macrophages after Leishmania and Trypanosoma cruzi infection. PLoS One, 2019, 14(12), e0225588.
[http://dx.doi.org/10.1371/journal.pone.0225588] [PMID: 31841511]
[26]
Fernandes, M.C.; Dillon, L.A.L.; Belew, A.T.; Bravo, H.C.; Mosser, D.M.; El-Sayed, N.M. Dual transcriptome profiling of Leishmania-infected human macrophages reveals distinct reprogramming signatures. MBio, 2016, 7(3), e00027-e16.
[http://dx.doi.org/10.1128/mBio.00027-16] [PMID: 27165796]
[27]
Gatto, M.; Borim, P.A.; Wolf, I.R.; Fukuta da Cruz, T.; Ferreira Mota, G.A.; Marques Braz, A.M.; Casella Amorim, B.; Targino Valente, G.; de Assis Golim, M.; Venturini, J.; Araújo Junior, J.P.; Pontillo, A.; Sartori, A. Transcriptional analysis of THP-1 cells infected with Leishmania infantum indicates no activation of the inflammasome platform. PLoS Negl. Trop. Dis., 2020, 14(1), e0007949.
[http://dx.doi.org/10.1371/journal.pntd.0007949] [PMID: 31961876]
[28]
Christensen, S.M.; Dillon, L.A.L.; Carvalho, L.P.; Passos, S.; Novais, F.O.; Hughitt, V.K.; Beiting, D.P.; Carvalho, E.M.; Scott, P.; El-Sayed, N.M.; Mosser, D.M. Meta-transcriptome profiling of the human-Leishmania braziliensis cutaneous lesion. PLoS Negl. Trop. Dis., 2016, 10(9), e0004992.
[http://dx.doi.org/10.1371/journal.pntd.0004992] [PMID: 27631090]
[29]
Rajkhowa, S.; Hazarika, Z.; Jha, A.N. Systems biology and bioinformatics approaches in leishmaniasis. In: Applications of Nanobiotechnology for Neglected Tropical Diseases; Academic Press: Cambridge, 2021; pp. 509-548.
[http://dx.doi.org/10.1016/B978-0-12-821100-7.00018-2]
[30]
Verma, A.; Bhandari, V.; Deep, D.K.; Sundar, S.; Dujardin, J.C.; Singh, R.; Salotra, P. Transcriptome profiling identifies genes/pathways associated with experimental resistance to paromomycin in Leishmania donovani. Int. J. Parasitol. Drugs Drug Resist., 2017, 7(3), 370-377.
[http://dx.doi.org/10.1016/j.ijpddr.2017.10.004] [PMID: 29035735]
[31]
Bhandari, V.; Sundar, S.; Dujardin, J.C.; Salotra, P. Elucidation of cellular mechanisms involved in experimental paromomycin resistance in Leishmania donovani. Antimicrob. Agents Chemother., 2014, 58(5), 2580-2585.
[http://dx.doi.org/10.1128/AAC.01574-13] [PMID: 24550335]
[32]
Medina, J.; Cruz-Saavedra, L.; Patiño, L.H.; Muñoz, M.; Ramírez, J.D. Comparative analysis of the transcriptional responses of five Leishmania species to trivalent antimony. Parasit. Vectors, 2021, 14(1), 419.
[http://dx.doi.org/10.1186/s13071-021-04915-y] [PMID: 34419127]
[33]
Baker, N.; Catta-Preta, C.M.C.; Neish, R.; Sadlova, J.; Powell, B.; Alves-Ferreira, E.V.C.; Geoghegan, V.; Carnielli, J.B.T.; Newling, K.; Hughes, C.; Vojtkova, B.; Anand, J.; Mihut, A.; Walrad, P.B.; Wilson, L.G.; Pitchford, J.W.; Volf, P.; Mottram, J.C. Systematic functional analysis of Leishmania protein kinases identifies regulators of differentiation or survival. Nat. Commun., 2021, 12(1), 1244.
[http://dx.doi.org/10.1038/s41467-021-21360-8] [PMID: 33623024]
[34]
Ayanlade, A.; Oluwaranti, A.; Ayanlade, O.S.; Borderon, M.; Sterly, H.; Sakdapolrak, P.; Jegede, M.O.; Weldemariam, L.F.; Ayinde, A.F.O. Extreme climate events in sub-Saharan Africa: A call for improving agricultural technology transfer to enhance adaptive capacity. Clim. Serv., 2022, 27, 100311.
[http://dx.doi.org/10.1016/j.cliser.2022.100311]
[35]
Anderson, B.A.; Wong, I.L.K.; Baugh, L.; Ramasamy, G.; Myler, P.J.; Beverley, S.M. Kinetoplastid-specific histone variant functions are conserved in Leishmania major. Mol. Biochem. Parasitol., 2013, 191(2), 53-57.
[http://dx.doi.org/10.1016/j.molbiopara.2013.09.005] [PMID: 24080031]
[36]
Roy, G.; Brar, H.K.; Muthuswami, R.; Madhubala, R. Epigenetic regulation of defense genes by histone deacetylase1 in human cell line-derived macrophages promotes intracellular survival of Leishmania donovani. PLoS Negl. Trop. Dis., 2020, 14(4), e0008167.
[http://dx.doi.org/10.1371/journal.pntd.0008167] [PMID: 32275661]
[37]
McDonald, J.R.; Jensen, B.C.; Sur, A.; Wong, I.L.K.; Beverley, S.M.; Myler, P.J. Localization of epigenetic markers in Leishmania chromatin. Pathogens, 2022, 11(8), 930.
[http://dx.doi.org/10.3390/pathogens11080930] [PMID: 36015053]
[38]
Piel, L.; Rajan, K.S.; Bussotti, G.; Varet, H.; Legendre, R.; Proux, C.; Douché, T.; Giai-Gianetto, Q.; Chaze, T.; Cokelaer, T.; Vojtkova, B.; Gordon-Bar, N.; Doniger, T.; Cohen-Chalamish, S.; Rengaraj, P.; Besse, C.; Boland, A.; Sadlova, J.; Deleuze, J.F.; Matondo, M.; Unger, R.; Volf, P.; Michaeli, S.; Pescher, P.; Späth, G.F. Experimental evolution links post-transcriptional regulation to Leishmania fitness gain. PLoS Pathog., 2022, 18(3), e1010375.
[http://dx.doi.org/10.1371/journal.ppat.1010375] [PMID: 35294501]
[39]
Marr, A.K.; MacIsaac, J.L.; Jiang, R.; Airo, A.M.; Kobor, M.S.; McMaster, W.R. Leishmania donovani infection causes distinct epigenetic DNA methylation changes in host macrophages. PLoS Pathog., 2014, 10(10), e1004419.
[http://dx.doi.org/10.1371/journal.ppat.1004419] [PMID: 25299267]
[40]
Lecoeur, H.; Prina, E.; Rosazza, T.; Kokou, K.; N’Diaye, P.; Aulner, N.; Varet, H.; Bussotti, G.; Xing, Y.; Milon, G. Targeting macrophage histone H3 modification as a Leishmania strategy to dampen the NF-κB/NLRP3-mediated inflammatory response. Cell Reports, 2020, 30(6), 1870-1882.e4.
[http://dx.doi.org/10.1016/j.celrep.2020.01.030] [PMID: 32049017]
[41]
Vega-Benedetti, A.F.; Loi, E.; Zavattari, P. DNA methylation alterations caused by Leishmania infection may generate a microenvironment prone to tumour development. Front. Cell. Infect. Microbiol., 2022, 12, 984134.
[http://dx.doi.org/10.3389/fcimb.2022.984134] [PMID: 36105147]
[42]
Brotherton, M.C.; Bourassa, S.; Leprohon, P.; Légaré, D.; Poirier, G.G.; Droit, A.; Ouellette, M. Proteomic and genomic analyses of antimony resistant Leishmania infantum mutant. PLoS One, 2013, 8(11), e81899.
[http://dx.doi.org/10.1371/journal.pone.0081899] [PMID: 24312377]
[43]
Akpunarlieva, S.; Weidt, S.; Lamasudin, D.; Naula, C.; Henderson, D.; Barrett, M.; Burgess, K.; Burchmore, R. Integration of proteomics and metabolomics to elucidate metabolic adaptation in Leishmania. J. Proteomics, 2017, 155, 85-98.
[http://dx.doi.org/10.1016/j.jprot.2016.12.009] [PMID: 28040509]
[44]
Amiri-Dashatan, N.; Rezaei-Tavirani, M.; Zali, H.; Koushki, M.; Ahmadi, N. Quantitative proteomic analysis reveals differentially expressed proteins in Leishmania major metacyclogenesis. Microb. Pathog., 2020, 149, 104557.
[http://dx.doi.org/10.1016/j.micpath.2020.104557] [PMID: 33017654]
[45]
Wheeler, R.J.; Gluenz, E.; Gull, K. The cell cycle of Leishmania: Morphogenetic events and their implications for parasite biology. Mol. Microbiol., 2011, 79(3), 647-662.
[http://dx.doi.org/10.1111/j.1365-2958.2010.07479.x] [PMID: 21255109]
[46]
Sanchiz, Á.; Morato, E.; Rastrojo, A.; Camacho, E.; González-de la Fuente, S.; Marina, A.; Aguado, B.; Requena, J.M. The experimental proteome of Leishmania infantum promastigote and its usefulness for improving gene annotations. Genes, 2020, 11(9), 1036.
[http://dx.doi.org/10.3390/genes11091036] [PMID: 32887454]
[47]
Negrão, F.; Fernandez-Costa, C.; Zorgi, N.; Giorgio, S.; Nogueira, E.M.; Yates, J.R. III Label-free proteomic analysis reveals parasite-specific protein alterations in macrophages following Leishmania amazonensis, Leishmania major, or Leishmania infantum Infection. ACS Infect. Dis., 2019, 5(6), 851-862.
[http://dx.doi.org/10.1021/acsinfecdis.8b00338] [PMID: 30978002]
[48]
Negreira, G.H.; Monsieurs, P.; Imamura, H.; Maes, I.; Kuk, N.; Yagoubat, A.; Van den Broeck, F.; Sterkers, Y.; Dujardin, J.C.; Domagalska, M.A. High throughput single-cell genome sequencing gives insights into the generation and evolution of mosaic aneuploidy in Leishmania donovani. Nucleic Acids Res., 2022, 50(1), 293-305.
[http://dx.doi.org/10.1093/nar/gkab1203] [PMID: 34893872]
[49]
Louradour, I.; Ferreira, T.R.; Duge, E.; Karunaweera, N.; Paun, A.; Sacks, D. Stress conditions promote Leishmania hybridization in vitro marked by expression of the ancestral gamete fusogen HAP2 as revealed by single-cell RNA-seq. eLife, 2022, 11, e73488.
[http://dx.doi.org/10.7554/eLife.73488] [PMID: 34994687]
[50]
Sharma, M.; Shaikh, N.; Yadav, S.; Singh, S.; Garg, P. A systematic reconstruction and constraint-based analysis of Leishmania donovani metabolic network: Identification of potential antileishmanial drug targets. Mol. Biosyst., 2017, 13(5), 955-969.
[http://dx.doi.org/10.1039/C6MB00823B] [PMID: 28367572]
[51]
Bora, N.; Nath Jha, A. An integrative approach using systems biology, mutational analysis with molecular dynamics simulation to challenge the functionality of a target protein. Chem. Biol. Drug Des., 2019, 93(6), cbdd.13502.
[http://dx.doi.org/10.1111/cbdd.13502] [PMID: 30891955]
[52]
Bora, N.; Jha, A.N. In silico Metabolic pathway analysis identifying target against leishmaniasis – a kinetic modeling approach. Front. Genet., 2020, 11, 179.
[http://dx.doi.org/10.3389/fgene.2020.00179] [PMID: 32211028]
[53]
Amiri-Dashatan, N.; Rezaei-Tavirani, M.; Ranjbar, M.M.; Koushki, M.; Nasab, S.D.M.; Ahmadi, N. Discovery of novel pyruvate kinase inhibitors in Leishmania major among FDA approved drugs through a system biology and molecular docking approach. Turkish J Pharm Sci, 2021, 18(6), 710-717.
[http://dx.doi.org/10.4274/tjps.galenos.2021.53367] [PMID: 34978400]
[54]
Akhoundi, M.; Downing, T.; Votýpka, J.; Kuhls, K.; Lukeš, J.; Cannet, A.; Ravel, C.; Marty, P.; Delaunay, P.; Kasbari, M.; Granouillac, B.; Gradoni, L.; Sereno, D. Leishmania infections: Molecular targets and diagnosis. Mol. Aspects Med., 2017, 57, 1-29.
[http://dx.doi.org/10.1016/j.mam.2016.11.012] [PMID: 28159546]
[55]
Ma, J.; Guo, Y.; Gao, J.; Tang, H.; Xu, K.; Liu, Q.; Xu, L. Climate change drives the transmission and spread of vector-borne diseases: An ecological perspective. Biology, 2022, 11(11), 1628.
[http://dx.doi.org/10.3390/biology11111628] [PMID: 36358329]
[56]
Charrahy, Z.; Yaghoobi-Ershadi, M.R.; Shirzadi, M.R.; Akhavan, A.A.; Rassi, Y.; Hosseini, S.Z.; Webb, N.J.; Haque, U.; Bozorg Omid, F.; Hanafi-Bojd, A.A. Climate change and its effect on the vulnerability to zoonotic cutaneous Leishmaniasis in Iran. Transbound. Emerg. Dis., 2022, 69(3), 1506-1520.
[http://dx.doi.org/10.1111/tbed.14115] [PMID: 33876891]
[57]
Moirano, G.; Ellena, M.; Mercogliano, P.; Richiardi, L.; Maule, M. Spatio-temporal pattern and meteo-climatic determinants of visceral leishmaniasis in Italy. Trop. Med. Infect. Dis., 2022, 7(11), 337.
[http://dx.doi.org/10.3390/tropicalmed7110337] [PMID: 36355879]
[58]
Daoudi, M.; Outammassine, A.; Amane, M.; Hafidi, M.; Boussaa, S.; Boumezzough, A. Climate change influences on the potential distribution of the sand fly Phlebotomus sergenti, vector of leishmania tropica in Morocco. Acta Parasitol., 2022, 67(2), 858-866.
[http://dx.doi.org/10.1007/s11686-022-00533-5] [PMID: 35294974]

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