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Current Topics in Medicinal Chemistry

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ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

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Current Frontiers

Contribution of Transcriptome to Elucidate the Biology of Plasmodium spp

Author(s): Kleber Simônio Parreira, Pedro Scarpelli, Wânia Rezende Lima* and Celia R.S. Garcia*

Volume 22, Issue 3, 2022

Published on: 11 January, 2022

Page: [169 - 187] Pages: 19

DOI: 10.2174/1568026622666220111140803

Price: $65

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Abstract

The present review discusses some of the new technologies that have been applied to elucidate how Plasmodium spp escape from the immune system and subvert the host physiology to orchestrate the regulation of its biological pathways. Our manuscript describes how techniques such as microarray approaches, RNA-Seq, and single-cell RNA sequencing have contributed to the discovery of transcripts and changed the concept of gene expression regulation in closely related malaria parasite species. Moreover, the text highlights the contributions of high-throughput RNA sequencing for the current knowledge of malaria parasite biology, physiology, vaccine target, and the revelation of new players in parasite signaling.

Keywords: Malaria, Plasmodium spp, Biologic process, RNA-Seq, Microarray, Single-cell RNA, Signaling pathway.

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Graphical Abstract

[1]
WHO World malaria report 2020: 20 years of global progress and challenges. World Health, 2020.
[2]
Bousema, T.; Drakeley, C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin. Microbiol. Rev., 2011, 24(2), 377-410.
[http://dx.doi.org/10.1128/CMR.00051-10] [PMID: 21482730]
[3]
Reis, P.A.; Estato, V.; da Silva, T.I.; d’Avila, J.C.; Siqueira, L.D.; Assis, E.F.; Bozza, P.T.; Bozza, F.A.; Tibiriça, E.V.; Zimmerman, G.A.; Castro-Faria-Neto, H.C. Statins decrease neuroinflammation and prevent cognitive impairment after cerebral malaria. PLoS Pathog., 2012, 8(12), e1003099.
[http://dx.doi.org/10.1371/journal.ppat.1003099] [PMID: 23300448]
[4]
Garcia, C.R.; de Azevedo, M.F.; Wunderlich, G.; Budu, A.; Young, J.A.; Bannister, L. Plasmodium in the postgenomic era: New insights into the molecular cell biology of malaria parasites. Int. Rev. Cell Mol. Biol., 2008, 266, 85-156.
[http://dx.doi.org/10.1016/S1937-6448(07)66003-1] [PMID: 18544493]
[5]
Bannister, L.H.; Hopkins, J.M.; Fowler, R.E.; Krishna, S.; Mitchell, G.H. Ultrastructure of rhoptry development in Plasmodium falciparum erythrocytic schizonts. Parasitology, 2000, 121(Pt 3), 273-287.
[http://dx.doi.org/10.1017/S0031182099006320] [PMID: 11085247]
[6]
Mita-Mendoza, N.K.; van de Hoef, D.L.; Lopera-Mesa, T.M.; Doumbia, S.; Konate, D.; Doumbouya, M.; Gu, W.; Anderson, J.M.; Santos-Argumedo, L.; Rodriguez, A.; Fay, M.P.; Diakite, M.; Long, C.A.; Fairhurst, R.M. A potential role for plasma uric acid in the endothelial pathology of Plasmodium falciparum malaria. PLoS One, 2013, 8(1), e54481.
[http://dx.doi.org/10.1371/journal.pone.0054481] [PMID: 23349902]
[7]
Carret, C.K.; Horrocks, P.; Konfortov, B.; Winzeler, E.; Qureshi, M.; Newbold, C.; Ivens, A. Microarray-based comparative genomic analyses of the human malaria parasite Plasmodium falciparum using Affymetrix arrays. Mol. Biochem. Parasitol., 2005, 144(2), 177-186.
[http://dx.doi.org/10.1016/j.molbiopara.2005.08.010] [PMID: 16174539]
[8]
Karnad, D.R.; Nor, M.B.M.; Richards, G.A.; Baker, T.; Amin, P. Council of the World Federation of Societies of Intensive and Critical Care Medicine. Intensive care in severe malaria: Report from the task force on tropical diseases by the World Federation of Societies of Intensive and Critical Care Medicine. J. Crit. Care, 2018, 43, 356-360.
[http://dx.doi.org/10.1016/j.jcrc.2017.11.007] [PMID: 29132978]
[9]
Val, F.; Avalos, S.; Gomes, A.A.; Zerpa, J.E.A.; Fontecha, G.; Siqueira, A.M.; Bassat, Q.; Alecrim, M.G.C.; Monteiro, W.M.; Lacerda, M.V.G. Are respiratory complications of Plasmodium vivax malaria an underestimated problem? Malar. J., 2017, 16(1), 495.
[http://dx.doi.org/10.1186/s12936-017-2143-y] [PMID: 29273053]
[10]
White, N.J.; Pukrittayakamee, S.; Hien, T.T.; Faiz, M.A.; Mokuolu, O.A.; Dondorp, A.M. Malaria. Lancet, 2014, 383(9918), 723-735.
[http://dx.doi.org/10.1016/S0140-6736(13)60024-0] [PMID: 23953767]
[11]
Bartoloni, A.; Zammarchi, L. Clinical aspects of uncomplicated and severe malaria. Mediterr. J. Hematol. Infect. Dis., 2012, 4(1), e2012026.
[http://dx.doi.org/10.4084/mjhid.2012.026] [PMID: 22708041]
[12]
Phyo, A.P.; Ashley, E.A.; Anderson, T.J.C.; Bozdech, Z.; Carrara, V.I.; Sriprawat, K.; Nair, S.; White, M.M.; Dziekan, J.; Ling, C.; Proux, S.; Konghahong, K.; Jeeyapant, A.; Woodrow, C.J.; Imwong, M.; McGready, R.; Lwin, K.M.; Day, N.P.J.; White, N.J.; Nosten, F. Declining efficacy of artemisinin combination therapy against P. falciparum malaria on the Thai-Myanmar border (2003-2013): The role of parasite genetic factors. Clin. Infect. Dis., 2016, 63(6), 784-791.
[http://dx.doi.org/10.1093/cid/ciw388] [PMID: 27313266]
[13]
Basilico, N.; Parapini, S.; Sparatore, A.; Romeo, S.; Misiano, P.; Vivas, L.; Yardley, V.; Croft, S.L.; Habluetzel, A.; Lucantoni, L.; Renia, L.; Russell, B.; Suwanarusk, R.; Nosten, F.; Dondio, G.; Bigogno, C.; Jabes, D.; Taramelli, D. In vivo and in vitro activities and adme-tox profile of a quinolizidine-modified 4-aminoquinoline: A potent anti-P. falciparum and anti-P. vivax blood-stage antimalarial. Molecules, 2017, 22(12), E2102.
[http://dx.doi.org/10.3390/molecules22122102] [PMID: 29194347]
[14]
Marques, M.M.; Costa, M.R.; Santana Filho, F.S.; Vieira, J.L.; Nascimento, M.T.; Brasil, L.W.; Nogueira, F.; Silveira, H.; Reyes-Lecca, R.C.; Monteiro, W.M.; Lacerda, M.V.; Alecrim, M.G. Plasmodium vivax chloroquine resistance and anemia in the western Brazilian Amazon. Antimicrob. Agents Chemother., 2014, 58(1), 342-347.
[http://dx.doi.org/10.1128/AAC.02279-12] [PMID: 24165179]
[15]
Uppal, K.; Salinas, J.L.; Monteiro, W.M.; Val, F.; Cordy, R.J.; Liu, K.; Melo, G.C.; Siqueira, A.M.; Magalhaes, B.; Galinski, M.R.; Lacerda, M.V.G.; Jones, D.P. Plasma metabolomics reveals membrane lipids, aspartate/asparagine and nucleotide metabolism pathway differences associated with chloroquine resistance in Plasmodium vivax malaria. PLoS One, 2017, 12(8), e0182819.
[http://dx.doi.org/10.1371/journal.pone.0182819] [PMID: 28813452]
[16]
Lowe, R.; Shirley, N.; Bleackley, M.; Dolan, S.; Shafee, T. Transcriptomics technologies. PLOS Comput. Biol., 2017, 13(5), e1005457.
[http://dx.doi.org/10.1371/journal.pcbi.1005457] [PMID: 28545146]
[17]
Gardner, M.J.; Hall, N.; Fung, E.; White, O.; Berriman, M.; Hyman, R.W.; Carlton, J.M.; Pain, A.; Nelson, K.E.; Bowman, S.; Paulsen, I.T.; James, K.; Eisen, J.A.; Rutherford, K.; Salzberg, S.L.; Craig, A.; Kyes, S.; Chan, M.S.; Nene, V.; Shallom, S.J.; Suh, B.; Peterson, J.; Angiuoli, S.; Pertea, M.; Allen, J.; Selengut, J.; Haft, D.; Mather, M.W.; Vaidya, A.B.; Martin, D.M.; Fairlamb, A.H.; Fraunholz, M.J.; Roos, D.S.; Ralph, S.A.; McFadden, G.I.; Cummings, L.M.; Subramanian, G.M.; Mungall, C.; Venter, J.C.; Carucci, D.J.; Hoffman, S.L.; Newbold, C.; Davis, R.W.; Fraser, C.M.; Barrell, B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, 2002, 419(6906), 498-511.
[http://dx.doi.org/10.1038/nature01097] [PMID: 12368864]
[18]
Hayward, R.E.; Derisi, J.L.; Alfadhli, S.; Kaslow, D.C.; Brown, P.O.; Rathod, P.K. Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol. Microbiol., 2000, 35(1), 6-14.
[http://dx.doi.org/10.1046/j.1365-2958.2000.01730.x] [PMID: 10632873]
[19]
Ben Mamoun, C.; Gluzman, I.Y.; Hott, C.; MacMillan, S.K.; Amarakone, A.S.; Anderson, D.L.; Carlton, J.M.; Dame, J.B.; Chakrabarti, D.; Martin, R.K.; Brownstein, B.H.; Goldberg, D.E. Co-ordinated programme of gene expression during asexual intraerythrocytic development of the human malaria parasite Plasmodium falciparum revealed by microarray analysis. Mol. Microbiol., 2001, 39(1), 26-36.
[http://dx.doi.org/10.1046/j.1365-2958.2001.02222.x] [PMID: 11123685]
[20]
Le Roch, K.G.; Zhou, Y.; Batalov, S.; Winzeler, E.A. Monitoring the chromosome 2 intraerythrocytic transcriptome of Plasmodium falciparum using oligonucleotide arrays. Am. J. Trop. Med. Hyg., 2002, 67(3), 233-243.
[http://dx.doi.org/10.4269/ajtmh.2002.67.233] [PMID: 12408661]
[21]
Bozdech, Z.; Mok, S.; Hu, G.; Imwong, M.; Jaidee, A.; Russell, B.; Ginsburg, H.; Nosten, F.; Day, N.P.; White, N.J.; Carlton, J.M.; Preiser, P.R. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc. Natl. Acad. Sci. USA, 2008, 105(42), 16290-16295.
[http://dx.doi.org/10.1073/pnas.0807404105] [PMID: 18852452]
[22]
Kaiser, K.; Matuschewski, K.; Camargo, N.; Ross, J.; Kappe, S.H. Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Mol. Microbiol., 2004, 51(5), 1221-1232.
[http://dx.doi.org/10.1046/j.1365-2958.2003.03909.x] [PMID: 14982620]
[23]
Hall, N.; Karras, M.; Raine, J.D.; Carlton, J.M.; Kooij, T.W.; Berriman, M.; Florens, L.; Janssen, C.S.; Pain, A.; Christophides, G.K.; James, K.; Rutherford, K.; Harris, B.; Harris, D.; Churcher, C.; Quail, M.A.; Ormond, D.; Doggett, J.; Trueman, H.E.; Mendoza, J.; Bidwell, S.L.; Rajandream, M.A.; Carucci, D.J.; Yates, J.R., III; Kafatos, F.C.; Janse, C.J.; Barrell, B.; Turner, C.M.; Waters, A.P.; Sinden, R.E. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science, 2005, 307(5706), 82-86.
[http://dx.doi.org/10.1126/science.1103717] [PMID: 15637271]
[24]
Liew, K.J.; Hu, G.; Bozdech, Z.; Peter, P.R. Defining species specific genome differences in malaria parasites. BMC Genomics, 2010, 11(1), 128.
[http://dx.doi.org/10.1186/1471-2164-11-128] [PMID: 20175934]
[25]
Tarun, A.S.; Peng, X.; Dumpit, R.F.; Ogata, Y.; Silva-Rivera, H.; Camargo, N.; Daly, T.M.; Bergman, L.W.; Kappe, S.H. A combined transcriptome and proteome survey of malaria parasite liver stages. Proc. Natl. Acad. Sci. USA, 2008, 105(1), 305-310.
[http://dx.doi.org/10.1073/pnas.0710780104] [PMID: 18172196]
[26]
Matuschewski, K.; Ross, J.; Brown, S.M.; Kaiser, K.; Nussenzweig, V.; Kappe, S.H. Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J. Biol. Chem., 2002, 277(44), 41948-41953.
[http://dx.doi.org/10.1074/jbc.M207315200] [PMID: 12177071]
[27]
Mikolajczak, S.A.; Silva-Rivera, H.; Peng, X.; Tarun, A.S.; Camargo, N.; Jacobs-Lorena, V.; Daly, T.M.; Bergman, L.W.; de la Vega, P.; Williams, J.; Aly, A.S.; Kappe, S.H. Distinct malaria parasite sporozoites reveal transcriptional changes that cause differential tissue infection competence in the mosquito vector and mammalian host. Mol. Cell. Biol., 2008, 28(20), 6196-6207.
[http://dx.doi.org/10.1128/MCB.00553-08] [PMID: 18710954]
[28]
Oakley, M.S.; Verma, N.; Myers, T.G.; Zheng, H.; Locke, E.; Morin, M.J.; Tripathi, A.K.; Mlambo, G.; Kumar, S. Transcriptome analysis based detection of Plasmodium falciparum development in Anopheles stephensi mosquitoes. Sci. Rep., 2018, 8(1), 11568.
[http://dx.doi.org/10.1038/s41598-018-29969-4] [PMID: 30068910]
[29]
LaMonte, G.M.; Orjuela-Sanchez, P.; Calla, J.; Wang, L.T.; Li, S.; Swann, J.; Cowell, A.N.; Zou, B.Y.; Abdel-Haleem Mohamed, A.M.; Villa Galarce, Z.H.; Moreno, M.; Tong Rios, C.; Vinetz, J.M.; Lewis, N.; Winzeler, E.A. Dual RNA-seq identifies human mucosal immunity protein Mucin-13 as a hallmark of Plasmodium exoerythrocytic infection. Nat. Commun., 2019, 10(1), 488.
[http://dx.doi.org/10.1038/s41467-019-08349-0] [PMID: 30700707]
[30]
Gómez-Díaz, E.; Yerbanga, R.S.; Lefèvre, T.; Cohuet, A.; Rowley, M.J.; Ouedraogo, J.B.; Corces, V.G. Epigenetic regulation of Plasmodium falciparum clonally variant gene expression during development in Anopheles gambiae. Sci. Rep., 2017, 7(1), 40655.
[http://dx.doi.org/10.1038/srep40655] [PMID: 28091569]
[31]
López-Barragán, M.J.; Lemieux, J.; Quiñones, M.; Williamson, K.C.; Molina-Cruz, A.; Cui, K.; Barillas-Mury, C.; Zhao, K.; Su, X.Z. Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics, 2011, 12(1), 587.
[http://dx.doi.org/10.1186/1471-2164-12-587] [PMID: 22129310]
[32]
Silvestrini, F.; Bozdech, Z.; Lanfrancotti, A.; Di Giulio, E.; Bultrini, E.; Picci, L.; Derisi, J.L.; Pizzi, E.; Alano, P. Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol. Biochem. Parasitol., 2005, 143(1), 100-110.
[http://dx.doi.org/10.1016/j.molbiopara.2005.04.015] [PMID: 16026866]
[33]
Young, J.A.; Fivelman, Q.L.; Blair, P.L.; de la Vega, P.; Le Roch, K.G.; Zhou, Y.; Carucci, D.J.; Baker, D.A.; Winzeler, E.A. The Plasmodium falciparum sexual development transcriptome: A microarray analysis using ontology-based pattern identification. Mol. Biochem. Parasitol., 2005, 143(1), 67-79.
[http://dx.doi.org/10.1016/j.molbiopara.2005.05.007] [PMID: 16005087]
[34]
Yeoh, L.M.; Goodman, C.D.; Mollard, V.; McFadden, G.I.; Ralph, S.A. Comparative transcriptomics of female and male gametocytes in Plasmodium berghei and the evolution of sex in alveolates. BMC Genomics, 2017, 18(1), 734.
[http://dx.doi.org/10.1186/s12864-017-4100-0] [PMID: 28923023]
[35]
Bozdech, Z.; Llinás, M.; Pulliam, B.L.; Wong, E.D.; Zhu, J.; DeRisi, J.L. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol., 2003, 1(1), E5.
[http://dx.doi.org/10.1371/journal.pbio.0000005] [PMID: 12929205]
[36]
Le Roch, K.G.; Johnson, J.R.; Florens, L.; Zhou, Y.; Santrosyan, A.; Grainger, M.; Yan, S.F.; Williamson, K.C.; Holder, A.A.; Carucci, D.J.; Yates, J.R., III; Winzeler, E.A. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res., 2004, 14(11), 2308-2318.
[http://dx.doi.org/10.1101/gr.2523904] [PMID: 15520293]
[37]
Shock, J.L.; Fischer, K.F.; DeRisi, J.L. Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol., 2007, 8(7), R134.
[http://dx.doi.org/10.1186/gb-2007-8-7-r134] [PMID: 17612404]
[38]
Zanghì, G.; Vembar, S.S.; Baumgarten, S.; Ding, S.; Guizetti, J.; Bryant, J.M.; Mattei, D.; Jensen, A.T.R.; Rénia, L.; Goh, Y.S.; Sauerwein, R.; Hermsen, C.C.; Franetich, J.F.; Bordessoulles, M.; Silvie, O.; Soulard, V.; Scatton, O.; Chen, P.; Mecheri, S.; Mazier, D.; Scherf, A. A specific PfEMP1 is expressed in P. falciparum sporozoites and plays a role in hepatocyte infection. Cell Rep., 2018, 22(11), 2951-2963.
[http://dx.doi.org/10.1016/j.celrep.2018.02.075] [PMID: 29539423]
[39]
Lasonder, E.; Rijpma, S.R.; van Schaijk, B.C.; Hoeijmakers, W.A.; Kensche, P.R.; Gresnigt, M.S.; Italiaander, A.; Vos, M.W.; Woestenenk, R.; Bousema, T.; Mair, G.R.; Khan, S.M.; Janse, C.J.; Bártfai, R.; Sauerwein, R.W. Integrated transcriptomic and proteomic analyses of P. falciparum gametocytes: Molecular insight into sex-specific processes and translational repression. Nucleic Acids Res., 2016, 44(13), 6087-6101.
[http://dx.doi.org/10.1093/nar/gkw536] [PMID: 27298255]
[40]
Toenhake, C.G.; Fraschka, S.A.; Vijayabaskar, M.S.; Westhead, D.R.; van Heeringen, S.J.; Bártfai, R. Chromatin accessibility-based characterization of the gene regulatory network underlying Plasmodium falciparum blood-stage development. Cell Host Microbe, 2018, 23(4), 557-569.e9.
[http://dx.doi.org/10.1016/j.chom.2018.03.007] [PMID: 29649445]
[41]
Tonkin, C.J.; Carret, C.K.; Duraisingh, M.T.; Voss, T.S.; Ralph, S.A.; Hommel, M.; Duffy, M.F.; Silva, L.M.; Scherf, A.; Ivens, A.; Speed, T.P.; Beeson, J.G.; Cowman, A.F. Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol., 2009, 7(4), e84.
[http://dx.doi.org/10.1371/journal.pbio.1000084] [PMID: 19402747]
[42]
Cubi, R.; Vembar, S.S.; Biton, A.; Franetich, J.F.; Bordessoulles, M.; Sossau, D.; Zanghi, G.; Bosson-Vanga, H.; Benard, M.; Moreno, A.; Dereuddre-Bosquet, N.; Le Grand, R.; Scherf, A.; Mazier, D. Laser capture microdissection enables transcriptomic analysis of dividing and quiescent liver stages of Plasmodium relapsing species. Cell. Microbiol., 2017, 19(8), e12735.
[http://dx.doi.org/10.1111/cmi.12735] [PMID: 28256794]
[43]
Kim, A.; Popovici, J.; Menard, D.; Serre, D. Plasmodium vivax transcriptomes reveal stage-specific chloroquine response and differential regulation of male and female gametocytes. Nat. Commun., 2019, 10(1), 371.
[http://dx.doi.org/10.1038/s41467-019-08312-z] [PMID: 30670687]
[44]
Witmer, K.; Schmid, C.D.; Brancucci, N.M.; Luah, Y.H.; Preiser, P.R.; Bozdech, Z.; Voss, T.S. Analysis of subtelomeric virulence gene families in Plasmodium falciparum by comparative transcriptional profiling. Mol. Microbiol., 2012, 84(2), 243-259.
[http://dx.doi.org/10.1111/j.1365-2958.2012.08019.x] [PMID: 22435676]
[45]
Painter, H.J.; Chung, N.C.; Sebastian, A.; Albert, I.; Storey, J.D.; Llinás, M. Genome-wide real-time in vivo transcriptional dynamics during Plasmodium falciparum blood-stage development. Nat. Commun., 2018, 9(1), 2656.
[http://dx.doi.org/10.1038/s41467-018-04966-3] [PMID: 29985403]
[46]
Mackinnon, M.J.; Li, J.; Mok, S.; Kortok, M.M.; Marsh, K.; Preiser, P.R.; Bozdech, Z. Comparative transcriptional and genomic analysis of Plasmodium falciparum field isolates. PLoS Pathog., 2009, 5(10), e1000644.
[http://dx.doi.org/10.1371/journal.ppat.1000644] [PMID: 19898609]
[47]
Rovira-Graells, N.; Gupta, A.P.; Planet, E.; Crowley, V.M.; Mok, S.; Ribas de Pouplana, L.; Preiser, P.R.; Bozdech, Z.; Cortés, A. Transcriptional variation in the malaria parasite Plasmodium falciparum. Genome Res., 2012, 22(5), 925-938.
[http://dx.doi.org/10.1101/gr.129692.111] [PMID: 22415456]
[48]
Kelemen, O.; Convertini, P.; Zhang, Z.; Wen, Y.; Shen, M.; Falaleeva, M.; Stamm, S. Function of alternative splicing. Gene, 2013, 514(1), 1-30.
[http://dx.doi.org/10.1016/j.gene.2012.07.083] [PMID: 22909801]
[49]
Iriko, H.; Jin, L.; Kaneko, O.; Takeo, S.; Han, E.T.; Tachibana, M.; Otsuki, H.; Torii, M.; Tsuboi, T. A small-scale systematic analysis of alternative splicing in Plasmodium falciparum. Parasitol. Int., 2009, 58(2), 196-199.
[http://dx.doi.org/10.1016/j.parint.2009.02.002] [PMID: 19268714]
[50]
Otto, T.D.; Wilinski, D.; Assefa, S.; Keane, T.M.; Sarry, L.R.; Böhme, U.; Lemieux, J.; Barrell, B.; Pain, A.; Berriman, M.; Newbold, C.; Llinás, M. New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol. Microbiol., 2010, 76(1), 12-24.
[http://dx.doi.org/10.1111/j.1365-2958.2009.07026.x] [PMID: 20141604]
[51]
Broadbent, K.M.; Broadbent, J.C.; Ribacke, U.; Wirth, D.; Rinn, J.L.; Sabeti, P.C. Strand-specific RNA sequencing in Plasmodium falciparum malaria identifies developmentally regulated long non- coding RNA and circular RNA. BMC Genomics, 2015, 16(1), 454.
[http://dx.doi.org/10.1186/s12864-015-1603-4] [PMID: 26070627]
[52]
Gabriel, H.B.; de Azevedo, M.F.; Palmisano, G.; Wunderlich, G.; Kimura, E.A.; Katzin, A.M.; Alves, J.M. Single-target high-throughput transcription analyses reveal high levels of alternative splicing present in the FPPS/GGPPS from Plasmodium falciparum. Sci. Rep., 2015, 5(1), 18429.
[http://dx.doi.org/10.1038/srep18429] [PMID: 26688062]
[53]
Zhu, L.; Mok, S.; Imwong, M.; Jaidee, A.; Russell, B.; Nosten, F.; Day, N.P.; White, N.J.; Preiser, P.R.; Bozdech, Z. New insights into the Plasmodium vivax transcriptome using RNA-Seq. Sci. Rep., 2016, 6(1), 20498.
[http://dx.doi.org/10.1038/srep20498] [PMID: 26858037]
[54]
Bártfai, R.; Hoeijmakers, W.A.; Salcedo-Amaya, A.M.; Smits, A.H.; Janssen-Megens, E.; Kaan, A.; Treeck, M.; Gilberger, T.W.; Françoijs, K.J.; Stunnenberg, H.G. H2A.Z demarcates intergenic regions of the Plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3. PLoS Pathog., 2010, 6(12), e1001223.
[http://dx.doi.org/10.1371/journal.ppat.1001223] [PMID: 21187892]
[55]
Sorber, K.; Dimon, M.T.; DeRisi, J.L. RNA-Seq analysis of splicing in Plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts. Nucleic Acids Res., 2011, 39(9), 3820-3835.
[http://dx.doi.org/10.1093/nar/gkq1223] [PMID: 21245033]
[56]
Wang, Z.; Gerstein, M.; Snyder, M. RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet., 2009, 10(1), 57-63.
[http://dx.doi.org/10.1038/nrg2484] [PMID: 19015660]
[57]
Angeletti, D.; Kiwuwa, M.S.; Byarugaba, J.; Kironde, F.; Wahlgren, M. Elevated levels of high-mobility group box-1 (HMGB1) in patients with severe or uncomplicated Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg., 2013, 88(4), 733-735.
[http://dx.doi.org/10.4269/ajtmh.12-0530] [PMID: 23400574]
[58]
Briquet, S.; Boschet, C.; Gissot, M.; Tissandié, E.; Sevilla, E.; Franetich, J.F.; Thiery, I.; Hamid, Z.; Bourgouin, C.; Vaquero, C. High-mobility-group box nuclear factors of Plasmodium falciparum. Eukaryot. Cell, 2006, 5(4), 672-682.
[http://dx.doi.org/10.1128/EC.5.4.672-682.2006] [PMID: 16607015]
[59]
Gissot, M.; Ting, L.M.; Daly, T.M.; Bergman, L.W.; Sinnis, P.; Kim, K. High mobility group protein HMGB2 is a critical regulator of Plasmodium oocyst development. J. Biol. Chem., 2008, 283(25), 17030-17038.
[http://dx.doi.org/10.1074/jbc.M801637200] [PMID: 18400754]
[60]
Lindner, S.E.; De Silva, E.K.; Keck, J.L.; Llinás, M. Structural determinants of DNA binding by a P. falciparum ApiAP2 transcriptional regulator. J. Mol. Biol., 2010, 395(3), 558-567.
[http://dx.doi.org/10.1016/j.jmb.2009.11.004] [PMID: 19913037]
[61]
Modrzynska, K.; Pfander, C.; Chappell, L.; Yu, L.; Suarez, C.; Dundas, K.; Gomes, A.R.; Goulding, D.; Rayner, J.C.; Choudhary, J.; Billker, O. A knockout screen of ApiAP2 genes reveals networks of interacting transcriptional regulators controlling the Plasmodium life cycle. Cell Host Microbe, 2017, 21(1), 11-22.
[http://dx.doi.org/10.1016/j.chom.2016.12.003] [PMID: 28081440]
[62]
Balaji, S.; Babu, M.M.; Iyer, L.M.; Aravind, L. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res., 2005, 33(13), 3994-4006.
[http://dx.doi.org/10.1093/nar/gki709] [PMID: 16040597]
[63]
Gissot, M.; Briquet, S.; Refour, P.; Boschet, C.; Vaquero, C. PfMyb1, a Plasmodium falciparum transcription factor, is required for intra-erythrocytic growth and controls key genes for cell cycle regulation. J. Mol. Biol., 2005, 346(1), 29-42.
[http://dx.doi.org/10.1016/j.jmb.2004.11.045] [PMID: 15663925]
[64]
Iwanaga, S.; Kaneko, I.; Kato, T.; Yuda, M. Identification of an AP2-family protein that is critical for malaria liver stage development. PLoS One, 2012, 7(11), e47557.
[http://dx.doi.org/10.1371/journal.pone.0047557] [PMID: 23144823]
[65]
Lima, W.R.; Martins, D.C.; Parreira, K.S.; Scarpelli, P.; Santos de Moraes, M.; Topalis, P.; Hashimoto, R.F.; Garcia, C.R.S. Genome-wide analysis of the human malaria parasite Plasmodium falciparum transcription factor PfNF-YB shows interaction with a CCAAT motif. Oncotarget, 2017, 8(69), 113987-114001.
[http://dx.doi.org/10.18632/oncotarget.23053] [PMID: 29371963]
[66]
Painter, H.J.; Campbell, T.L.; Llinás, M. The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol. Biochem. Parasitol., 2011, 176(1), 1-7.
[http://dx.doi.org/10.1016/j.molbiopara.2010.11.014] [PMID: 21126543]
[67]
Yuda, M.; Iwanaga, S.; Kaneko, I.; Kato, T. Global transcriptional repression: An initial and essential step for Plasmodium sexual development. Proc. Natl. Acad. Sci. USA, 2015, 112(41), 12824-12829.
[http://dx.doi.org/10.1073/pnas.1504389112] [PMID: 26417110]
[68]
Tuteja, R.; Ansari, A.; Chauhan, V.S. Emerging functions of transcription factors in malaria parasite. J. Biomed. Biotechnol., 2011, 2011, 461979.
[http://dx.doi.org/10.1155/2011/461979] [PMID: 22131806]
[69]
Caro, F.; Ahyong, V.; Betegon, M.; DeRisi, J.L. Genome-wide regulatory dynamics of translation in the Plasmodium falciparum asexual blood stages. eLife, 2014, 3, 3.
[http://dx.doi.org/10.7554/eLife.04106] [PMID: 25493618]
[70]
Bunnik, E.M.; Batugedara, G.; Saraf, A.; Prudhomme, J.; Florens, L.; Le Roch, K.G. The mRNA-bound proteome of the human malaria parasite Plasmodium falciparum. Genome Biol., 2016, 17(1), 147.
[http://dx.doi.org/10.1186/s13059-016-1014-0] [PMID: 27381095]
[71]
Yang, M.; Shang, X.; Zhou, Y.; Wang, C.; Wei, G.; Tang, J.; Zhang, M.; Liu, Y.; Cao, J.; Zhang, Q. Full-length transcriptome analysis of Plasmodium falciparum by single-molecule long-read sequencing. Front. Cell. Infect. Microbiol., 2021, 11, 631545.
[http://dx.doi.org/10.3389/fcimb.2021.631545] [PMID: 33708645]
[72]
Foth, B.J.; Zhang, N.; Chaal, B.K.; Sze, S.K.; Preiser, P.R.; Bozdech, Z. Quantitative time-course profiling of parasite and host cell proteins in the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics, 2011, 10(8), M110-6411.
[http://dx.doi.org/10.1074/mcp.M110.006411]
[73]
Nirmalan, N.; Sims, P.F.; Hyde, J.E. Quantitative proteomics of the human malaria parasite Plasmodium falciparum and its application to studies of development and inhibition. Mol. Microbiol., 2004, 52(4), 1187-1199.
[http://dx.doi.org/10.1111/j.1365-2958.2004.04049.x] [PMID: 15130134]
[74]
Foth, B.J.; Zhang, N.; Mok, S.; Preiser, P.R.; Bozdech, Z. Quantitative protein expression profiling reveals extensive post-transcriptional regulation and post-translational modifications in schizont-stage malaria parasites. Genome Biol., 2008, 9(12), R177.
[http://dx.doi.org/10.1186/gb-2008-9-12-r177] [PMID: 19091060]
[75]
Chaal, B.K.; Gupta, A.P.; Wastuwidyaningtyas, B.D.; Luah, Y.H.; Bozdech, Z. Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog., 2010, 6(1), e1000737.
[http://dx.doi.org/10.1371/journal.ppat.1000737] [PMID: 20107518]
[76]
Cui, L.; Miao, J.; Furuya, T.; Fan, Q.; Li, X.; Rathod, P.K.; Su, X.Z.; Cui, L. Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development. Eukaryot. Cell, 2008, 7(7), 1200-1210.
[http://dx.doi.org/10.1128/EC.00063-08] [PMID: 18487348]
[77]
Otto, T.D.; Böhme, U.; Jackson, A.P.; Hunt, M.; Franke-Fayard, B.; Hoeijmakers, W.A.; Religa, A.A.; Robertson, L.; Sanders, M.; Ogun, S.A.; Cunningham, D.; Erhart, A.; Billker, O.; Khan, S.M.; Stunnenberg, H.G.; Langhorne, J.; Holder, A.A.; Waters, A.P.; Newbold, C.I.; Pain, A.; Berriman, M.; Janse, C.J. A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol., 2014, 12(1), 86.
[http://dx.doi.org/10.1186/s12915-014-0086-0] [PMID: 25359557]
[78]
Warncke, J.D.; Vakonakis, I.; Beck, H.P. Plasmodium Helical Interspersed Subtelomeric (PHIST) proteins, at the center of host cell remodeling. Microbiol. Mol. Biol. Rev., 2016, 80(4), 905-927.
[http://dx.doi.org/10.1128/MMBR.00014-16] [PMID: 27582258]
[79]
Gunalan, K.; Gao, X.; Yap, S.S.; Huang, X.; Preiser, P.R. The role of the reticulocyte-binding-like protein homologues of Plasmodium in erythrocyte sensing and invasion. Cell. Microbiol., 2013, 15(1), 35-44.
[http://dx.doi.org/10.1111/cmi.12038] [PMID: 23046317]
[80]
Swapna, L.S.; Parkinson, J. Genomics of apicomplexan parasites. Crit. Rev. Biochem. Mol. Biol., 2017, 52(3), 254-273.
[http://dx.doi.org/10.1080/10409238.2017.1290043] [PMID: 28276701]
[81]
Fraschka, S.A.; Filarsky, M.; Hoo, R.; Niederwieser, I.; Yam, X.Y.; Brancucci, N.M.B.; Mohring, F.; Mushunje, A.T.; Huang, X.; Christensen, P.R.; Nosten, F.; Bozdech, Z.; Russell, B.; Moon, R.W.; Marti, M.; Preiser, P.R.; Bártfai, R.; Voss, T.S. Comparative heterochromatin profiling reveals conserved and unique epigenome signatures linked to adaptation and development of malaria parasites. Cell Host Microbe, 2018, 23(3), 407-420.e8.
[http://dx.doi.org/10.1016/j.chom.2018.01.008] [PMID: 29503181]
[82]
Rashidi, M.; Tavalaee, M.; Abbasi, H.; Nomikos, M.; Nasr-Esfahani, M.H. Increased de novo DNA methylation enzymes in sperm of individuals with varicocele. Cell J., 2021, 23(4), 389-396.
[PMID: 34455713]
[83]
Cortés, A.; Deitsch, K.W. Malaria epigenetics. Cold Spring Harb. Perspect. Med., 2017, 7(7), a025528.
[http://dx.doi.org/10.1101/cshperspect.a025528] [PMID: 28320828]
[84]
Hollin, T.; Gupta, M.; Lenz, T.; Le Roch, K.G. Dynamic chromatin structure and epigenetics control the fate of malaria parasites. Trends Genet., 2021, 37(1), 73-85.
[http://dx.doi.org/10.1016/j.tig.2020.09.003] [PMID: 32988634]
[85]
Bozdech, Z.; Zhu, J.; Joachimiak, M.P.; Cohen, F.E.; Pulliam, B.; DeRisi, J.L. Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biol., 2003, 4(2), R9.
[http://dx.doi.org/10.1186/gb-2003-4-2-r9] [PMID: 12620119]
[86]
Daily, J.P.; Scanfeld, D.; Pochet, N.; Le Roch, K.; Plouffe, D.; Kamal, M.; Sarr, O.; Mboup, S.; Ndir, O.; Wypij, D.; Levasseur, K.; Thomas, E.; Tamayo, P.; Dong, C.; Zhou, Y.; Lander, E.S.; Ndiaye, D.; Wirth, D.; Winzeler, E.A.; Mesirov, J.P.; Regev, A. Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature, 2007, 450(7172), 1091-1095.
[http://dx.doi.org/10.1038/nature06311] [PMID: 18046333]
[87]
Hoo, R.; Bruske, E.; Dimonte, S.; Zhu, L.; Mordmüller, B.; Sim, B.K.L.; Kremsner, P.G.; Hoffman, S.L.; Bozdech, Z.; Frank, M.; Preiser, P.R. Transcriptome profiling reveals functional variation in Plasmodium falciparum parasites from controlled human malaria infection studies. EBioMedicine, 2019, 48, 442-452.
[http://dx.doi.org/10.1016/j.ebiom.2019.09.001] [PMID: 31521613]
[88]
Boldt, A.B.W.; van Tong, H.; Grobusch, M.P.; Kalmbach, Y.; Dzeing Ella, A.; Kombila, M.; Meyer, C.G.; Kun, J.F.J.; Kremsner, P.G.; Velavan, T.P. The blood transcriptome of childhood malaria. EBioMedicine, 2019, 40, 614-625.
[http://dx.doi.org/10.1016/j.ebiom.2018.12.055] [PMID: 30638864]
[89]
Prajapati, S.K.; Ayanful-Torgby, R.; Pava, Z.; Barbeau, M.C.; Acquah, F.K.; Cudjoe, E.; Kakaney, C.; Amponsah, J.A.; Obboh, E.; Ahmed, A.E.; Abuaku, B.K.; McCarthy, J.S.; Amoah, L.E.; Williamson, K.C. The transcriptome of circulating sexually committed Plasmodium falciparum ring stage parasites forecasts malaria transmission potential. Nat. Commun., 2020, 11(1), 6159.
[http://dx.doi.org/10.1038/s41467-020-19988-z] [PMID: 33268801]
[90]
Siegel, S.V.; Rayner, J.C. Single cell sequencing shines a light on malaria parasite relatedness in complex infections. Trends Parasitol., 2020, 36(2), 83-85.
[http://dx.doi.org/10.1016/j.pt.2019.12.007] [PMID: 31883706]
[91]
Bourgard, C.; Lopes, S.C.P.; Lacerda, M.V.G.; Albrecht, L.; Costa, F.T.M. A suitable RNA preparation methodology for whole transcriptome shotgun sequencing harvested from Plasmodium vivax-infected patients. Sci. Rep., 2021, 11(1), 5089.
[http://dx.doi.org/10.1038/s41598-021-84607-w] [PMID: 33658571]
[92]
Nussenzweig, R.S.; Vanderberg, J.; Most, H.; Orton, C. Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature, 1967, 216(5111), 160-162.
[http://dx.doi.org/10.1038/216160a0] [PMID: 6057225]
[93]
Florens, L.; Washburn, M.P.; Raine, J.D.; Anthony, R.M.; Grainger, M.; Haynes, J.D.; Moch, J.K.; Muster, N.; Sacci, J.B.; Tabb, D.L.; Witney, A.A.; Wolters, D.; Wu, Y.; Gardner, M.J.; Holder, A.A.; Sinden, R.E.; Yates, J.R.; Carucci, D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature, 2002, 419(6906), 520-526.
[http://dx.doi.org/10.1038/nature01107] [PMID: 12368866]
[94]
Bettencourt, P. Current challenges in the identification of pre-erythrocytic malaria vaccine candidate antigens. Front. Immunol., 2020, 11, 190.
[http://dx.doi.org/10.3389/fimmu.2020.00190] [PMID: 32153565]
[95]
Siau, A.; Silvie, O.; Franetich, J.F.; Yalaoui, S.; Marinach, C.; Hannoun, L.; van Gemert, G.J.; Luty, A.J.; Bischoff, E.; David, P.H.; Snounou, G.; Vaquero, C.; Froissard, P.; Mazier, D. Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection. PLoS Pathog., 2008, 4(8), e1000121.
[http://dx.doi.org/10.1371/journal.ppat.1000121] [PMID: 18688281]
[96]
Williams, C.T.; Azad, A.F. Transcriptional analysis of the pre-erythrocytic stages of the rodent malaria parasite, Plasmodium yoelii. PLoS One, 2010, 5(4), e10267.
[http://dx.doi.org/10.1371/journal.pone.0010267] [PMID: 20422005]
[97]
Trieu, A.; Kayala, M.A.; Burk, C.; Molina, D.M.; Freilich, D.A.; Richie, T.L.; Baldi, P.; Felgner, P.L.; Doolan, D.L. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol Cell Proteomics, 2011, 10(9), M111 007948.
[98]
Aguiar, J.C.; Bolton, J.; Wanga, J.; Sacci, J.B.; Iriko, H.; Mazeika, J.K.; Han, E.T.; Limbach, K.; Patterson, N.B.; Sedegah, M.; Cruz, A.M.; Tsuboi, T.; Hoffman, S.L.; Carucci, D.; Hollingdale, M.R.; Villasante, E.D.; Richie, T.L. Discovery of novel Plasmodium falciparum pre-erythrocytic antigens for vaccine development. PLoS One, 2015, 10(8), e0136109.
[http://dx.doi.org/10.1371/journal.pone.0136109] [PMID: 26292257]
[99]
Speake, C.; Pichugin, A.; Sahu, T.; Malkov, V.; Morrison, R.; Pei, Y.; Juompan, L.; Milman, N.; Zarling, S.; Anderson, C.; MacDonald, N.J.; Wong-Madden, S.; Wendler, J.; Ishizuka, A.; MacMillen, Z.W.; Garcia, V.; Kappe, S.H.; Krzych, U.; Duffy, P.E. Correction: Identification of novel pre-erythrocytic malaria antigen candidates for combination vaccines with circumsporozoite protein. PLoS One, 2016, 11(10), e0165489.
[http://dx.doi.org/10.1371/journal.pone.0165489] [PMID: 27764243]
[100]
Speake, C.; Pichugin, A.; Sahu, T.; Malkov, V.; Morrison, R.; Pei, Y.; Juompan, L.; Milman, N.; Zarling, S.; Anderson, C.; Wong- Madden, S.; Wendler, J.; Ishizuka, A.; MacMillen, Z.W.; Garcia, V.; Kappe, S.H.; Krzych, U.; Duffy, P.E. Identification of novel pre-erythrocytic malaria antigen candidates for combination vaccines with circumsporozoite protein. PLoS One, 2016, 11(7), e0159449.
[http://dx.doi.org/10.1371/journal.pone.0159449] [PMID: 27434123]
[101]
Rts, S.C.T.P. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: Final results of a phase 3, individually randomised, controlled trial. Lancet, 2015, 386(9988), 31-45.
[http://dx.doi.org/10.1016/S0140-6736(15)60721-8] [PMID: 25913272]
[102]
Chandramohan, D.; Zongo, I.; Sagara, I.; Cairns, M.; Yerbanga, R.S.; Diarra, M.; Nikièma, F.; Tapily, A.; Sompougdou, F.; Issiaka, D.; Zoungrana, C.; Sanogo, K.; Haro, A.; Kaya, M.; Sienou, A.A.; Traore, S.; Mahamar, A.; Thera, I.; Diarra, K.; Dolo, A.; Kuepfer, I.; Snell, P.; Milligan, P.; Ockenhouse, C.; Ofori-Anyinam, O.; Tinto, H.; Djimde, A.; Ouédraogo, J.B.; Dicko, A.; Greenwood, B. Seasonal malaria vaccination with or without seasonal malaria chemoprevention. N. Engl. J. Med., 2021, 385(11), 1005-1017.
[http://dx.doi.org/10.1056/NEJMoa2026330] [PMID: 34432975]
[103]
Moncunill, G.; Scholzen, A.; Mpina, M.; Nhabomba, A.; Hounkpatin, A.B.; Osaba, L.; Valls, R.; Campo, J.J.; Sanz, H.; Jairoce, C.; Williams, N.A.; Pasini, E.M.; Arteta, D.; Maynou, J.; Palacios, L.; Duran-Frigola, M.; Aponte, J.J.; Kocken, C.H.M.; Agnandji, S.T.; Mas, J.M.; Mordmüller, B.; Daubenberger, C.; Sauerwein, R.; Dobaño, C. Antigen-stimulated PBMC transcriptional protective signatures for malaria immunization. Sci. Transl. Med., 2020, 12(543), eaay8924.
[http://dx.doi.org/10.1126/scitranslmed.aay8924] [PMID: 32404508]
[104]
Du, Y.; Thompson, E.G.; Muller, J.; Valvo, J.; Braun, J.; Shankar, S.; van den Berg, R.A.; Jongert, E.; Dover, D.; Sadoff, J.; Hendriks, J.; Gardner, M.J.; Ballou, W.R.; Regules, J.A.; van der Most, R.; Aderem, A.; Ockenhouse, C.F.; Hill, A.V.; Wille-Reece, U.; Zak, D.E. The ratiometric transcript signature MX2/GPR183 is consistently associated with RTS,S-mediated protection against controlled human malaria infection. Front. Immunol., 2020, 11, 669.
[http://dx.doi.org/10.3389/fimmu.2020.00669] [PMID: 32411130]
[105]
Daily, J.P.; Le Roch, K.G.; Sarr, O.; Fang, X.; Zhou, Y.; Ndir, O.; Mboup, S.; Sultan, A.; Winzeler, E.A.; Wirth, D.F. In vivo transcriptional profiling of Plasmodium falciparum. Malar. J., 2004, 3(1), 30.
[http://dx.doi.org/10.1186/1475-2875-3-30] [PMID: 15296511]
[106]
Llinás, M.; Bozdech, Z.; Wong, E.D.; Adai, A.T.; DeRisi, J.L. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res., 2006, 34(4), 1166-1173.
[http://dx.doi.org/10.1093/nar/gkj517] [PMID: 16493140]
[107]
Zhao, W.; Dauwels, J.; Cao, J. The effects of cell asynchrony on time-series data: An analysis on gene expression level of Plasmodium falciparum. Conf. Proc. IEEE Eng. Med. Biol. Soc., 2014, 2014, 5224-5227.
[PMID: 25571171]
[108]
Antony, H.A.; Pathak, V.; Parija, S.C.; Ghosh, K.; Bhattacherjee, A. Transcriptomic analysis of chloroquine-sensitive and chloroquine-resistant strains of Plasmodium falciparum: Toward malaria diagnostics and therapeutics for global health. OMICS, 2016, 20(7), 424-432.
[http://dx.doi.org/10.1089/omi.2016.0058] [PMID: 27428254]
[109]
Gunasekera, A.M.; Myrick, A.; Le Roch, K.; Winzeler, E.; Wirth, D.F. Plasmodium falciparum: Genome wide perturbations in transcript profiles among mixed stage cultures after chloroquine treatment. Exp. Parasitol., 2007, 117(1), 87-92.
[http://dx.doi.org/10.1016/j.exppara.2007.03.001] [PMID: 17475254]
[110]
Mattick, J.S.; Makunin, I.V. Small regulatory RNAs in mammals. Hum. Mol. Genet., 2005, 14(Spec No 1)(Suppl. 1), R121-R132.
[http://dx.doi.org/10.1093/hmg/ddi101] [PMID: 15809264]
[111]
Barker, K.R.; Lu, Z.; Kim, H.; Zheng, Y.; Chen, J.; Conroy, A.L.; Hawkes, M.; Cheng, H.S.; Njock, M.S.; Fish, J.E.; Harlan, J.M.; López, J.A.; Liles, W.C.; Kain, K.C. miR-155 modifies inflammation, endothelial activation and blood-brain barrier dysfunction in cerebral malaria. Mol. Med., 2017, 23(1), 24-33.
[http://dx.doi.org/10.2119/molmed.2016.00139] [PMID: 28182191]
[112]
LaMonte, G.; Philip, N.; Reardon, J.; Lacsina, J.R.; Majoros, W.; Chapman, L.; Thornburg, C.D.; Telen, M.J.; Ohler, U.; Nicchitta, C.V.; Haystead, T.; Chi, J.T. Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe, 2012, 12(2), 187-199.
[http://dx.doi.org/10.1016/j.chom.2012.06.007] [PMID: 22901539]
[113]
Mantel, P.Y.; Hjelmqvist, D.; Walch, M.; Kharoubi-Hess, S.; Nilsson, S.; Ravel, D.; Ribeiro, M.; Grüring, C.; Ma, S.; Padmanabhan, P.; Trachtenberg, A.; Ankarklev, J.; Brancucci, N.M.; Huttenhower, C.; Duraisingh, M.T.; Ghiran, I.; Kuo, W.P.; Filgueira, L.; Martinelli, R.; Marti, M. Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria. Nat. Commun., 2016, 7(1), 12727.
[http://dx.doi.org/10.1038/ncomms12727] [PMID: 27721445]
[114]
Guizetti, J.; Barcons-Simon, A.; Scherf, A. Trans-acting GC-rich non-coding RNA at var expression site modulates gene counting in malaria parasite. Nucleic Acids Res., 2016, 44(20), 9710-9718.
[PMID: 27466391]
[115]
Wei, G.; Zhao, Y.; Zhang, Q.; Pan, W. Dual regulatory effects of non-coding GC-rich elements on the expression of virulence genes in malaria parasites. Infect. Genet. Evol., 2015, 36, 490-499.
[http://dx.doi.org/10.1016/j.meegid.2015.08.023] [PMID: 26299885]
[116]
Subudhi, A.K.; Boopathi, P.A.; Garg, S.; Middha, S.; Acharya, J.; Pakalapati, D.; Saxena, V.; Aiyaz, M.; Orekondy, H.B.; Mugasimangalam, R.C.; Sirohi, P.; Kochar, S.K.; Kochar, D.K.; Das, A. An in vivo transcriptome data set of natural antisense transcripts from Plasmodium falciparum clinical isolates. Genom. Data, 2014, 2, 393-395.
[http://dx.doi.org/10.1016/j.gdata.2014.10.010] [PMID: 26484136]
[117]
Subudhi, A.K.; Boopathi, P.A.; Garg, S.; Middha, S.; Acharya, J.; Pakalapati, D.; Saxena, V.; Aiyaz, M.; Orekondy, H.B.; Mugasimangalam, R.C.; Sirohi, P.; Kochar, S.K.; Kochar, D.K.; Das, A. Natural antisense transcripts in Plasmodium falciparum isolates from patients with complicated malaria. Exp. Parasitol., 2014, 141, 39-54.
[http://dx.doi.org/10.1016/j.exppara.2014.03.008] [PMID: 24657575]
[118]
Deitsch, K.W.; Dzikowski, R. Variant gene expression and antigenic variation by malaria parasites. Annu. Rev. Microbiol., 2017, 71(1), 625-641.
[http://dx.doi.org/10.1146/annurev-micro-090816-093841] [PMID: 28697665]
[119]
Beeson, J.G.; Chan, J.A.; Fowkes, F.J. PfEMP1 as a target of human immunity and a vaccine candidate against malaria. Expert Rev. Vaccines, 2013, 12(2), 105-108.
[http://dx.doi.org/10.1586/erv.12.144] [PMID: 23414401]
[120]
Bull, P.C.; Abdi, A.I. The role of PfEMP1 as targets of naturally acquired immunity to childhood malaria: prospects for a vaccine. Parasitology, 2016, 143(2), 171-186.
[http://dx.doi.org/10.1017/S0031182015001274] [PMID: 26741401]
[121]
Boopathi, P.A.; Subudhi, A.K.; Garg, S.; Middha, S.; Acharya, J.; Pakalapati, D.; Saxena, V.; Aiyaz, M.; Chand, B.; Mugasimangalam, R.C.; Kochar, S.K.; Sirohi, P.; Kochar, D.K.; Das, A. Revealing natural antisense transcripts from Plasmodium vivax isolates: evidence of genome regulation in complicated malaria. Infect. Genet. Evol., 2013, 20, 428-443.
[http://dx.doi.org/10.1016/j.meegid.2013.09.026] [PMID: 24121022]
[122]
Winter, F.; Edaye, S.; Hüttenhofer, A.; Brunel, C. Anopheles gambiae miRNAs as actors of defence reaction against Plasmodium invasion. Nucleic Acids Res., 2007, 35(20), 6953-6962.
[http://dx.doi.org/10.1093/nar/gkm686] [PMID: 17933784]
[123]
Howick, V.M.; Russell, A.J.C.; Andrews, T.; Heaton, H.; Reid, A.J.; Natarajan, K.; Butungi, H.; Metcalf, T.; Verzier, L.H.; Rayner, J.C.; Berriman, M.; Herren, J.K.; Billker, O.; Hemberg, M.; Talman, A.M.; Lawniczak, M.K.N. The Malaria Cell Atlas: Single parasite transcriptomes across the complete Plasmodium life cycle. Science, 2019, 365(6455), eaaw2619.
[http://dx.doi.org/10.1126/science.aaw2619] [PMID: 31439762]
[124]
Real, E.; Howick, V.M.; Dahalan, F.A.; Witmer, K.; Cudini, J.; Andradi-Brown, C.; Blight, J.; Davidson, M.S.; Dogga, S.K.; Reid, A.J.; Baum, J.; Lawniczak, M.K.N. A single-cell atlas of Plasmodium falciparum transmission through the mosquito. Nat. Commun., 2021, 12(1), 3196.
[http://dx.doi.org/10.1038/s41467-021-23434-z] [PMID: 34045457]
[125]
Ruberto, A.A.; Bourke, C.; Merienne, N.; Obadia, T.; Amino, R.; Mueller, I. Single-cell RNA sequencing reveals developmental heterogeneity among Plasmodium berghei sporozoites. Sci. Rep., 2021, 11(1), 4127.
[http://dx.doi.org/10.1038/s41598-021-82914-w] [PMID: 33619283]
[126]
Haber, A.L.; Biton, M.; Rogel, N.; Herbst, R.H.; Shekhar, K.; Smillie, C.; Burgin, G.; Delorey, T.M.; Howitt, M.R.; Katz, Y.; Tirosh, I.; Beyaz, S.; Dionne, D.; Zhang, M.; Raychowdhury, R.; Garrett, W.S.; Rozenblatt-Rosen, O.; Shi, H.N.; Yilmaz, O.; Xavier, R.J.; Regev, A. A single-cell survey of the small intestinal epithelium. Nature, 2017, 551(7680), 333-339.
[http://dx.doi.org/10.1038/nature24489] [PMID: 29144463]
[127]
Grün, D.; Lyubimova, A.; Kester, L.; Wiebrands, K.; Basak, O.; Sasaki, N.; Clevers, H.; van Oudenaarden, A. Single-cell messenger RNA sequencing reveals rare intestinal cell types. Nature, 2015, 525(7568), 251-255.
[http://dx.doi.org/10.1038/nature14966] [PMID: 26287467]
[128]
Mohammed, H.; Hernando-Herraez, I.; Savino, A.; Scialdone, A.; Macaulay, I.; Mulas, C.; Chandra, T.; Voet, T.; Dean, W.; Nichols, J.; Marioni, J.C.; Reik, W. Single-cell landscape of transcriptional heterogeneity and cell fate decisions during mouse early gastrulation. Cell Rep., 2017, 20(5), 1215-1228.
[http://dx.doi.org/10.1016/j.celrep.2017.07.009] [PMID: 28768204]
[129]
Kafsack, B.F.; Rovira-Graells, N.; Clark, T.G.; Bancells, C.; Crowley, V.M.; Campino, S.G.; Williams, A.E.; Drought, L.G.; Kwiatkowski, D.P.; Baker, D.A.; Cortés, A.; Llinás, M. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature, 2014, 507(7491), 248-252.
[http://dx.doi.org/10.1038/nature12920] [PMID: 24572369]
[130]
Sinha, S.; Medhi, B.; Sehgal, R. Challenges of drug-resistant malaria. Parasite, 2014, 21, 61.
[http://dx.doi.org/10.1051/parasite/2014059] [PMID: 25402734]
[131]
Tembo, D.L.; Nyoni, B.; Murikoli, R.V.; Mukaka, M.; Milner, D.A.; Berriman, M.; Rogerson, S.J.; Taylor, T.E.; Molyneux, M.E.; Mandala, W.L.; Craig, A.G.; Montgomery, J. Differential PfEMP1 expression is associated with cerebral malaria pathology. PLoS Pathog., 2014, 10(12), e1004537.
[http://dx.doi.org/10.1371/journal.ppat.1004537] [PMID: 25473835]
[132]
Scherf, A.; Rivière, L.; Lopez-Rubio, J.J. SnapShot: var gene expression in the malaria parasite. Cell, 2008, 134(1), 190-190.e1.
[http://dx.doi.org/10.1016/j.cell.2008.06.042] [PMID: 18614021]
[133]
Brancucci, N.M.B.; De Niz, M.; Straub, T.J.; Ravel, D.; Sollelis, L.; Birren, B.W.; Voss, T.S.; Neafsey, D.E.; Marti, M. Probing Plasmodium falciparum sexual commitment at the single-cell level. Wellcome Open Res., 2018, 3, 70.
[http://dx.doi.org/10.12688/wellcomeopenres.14645.4] [PMID: 30320226]
[134]
Poran, A.; Nötzel, C.; Aly, O.; Mencia-Trinchant, N.; Harris, C.T.; Guzman, M.L.; Hassane, D.C.; Elemento, O.; Kafsack, B.F.C. Single-cell RNA sequencing reveals a signature of sexual commitment in malaria parasites. Nature, 2017, 551(7678), 95-99.
[http://dx.doi.org/10.1038/nature24280] [PMID: 29094698]
[135]
Reid, A.J.; Talman, A.M.; Bennett, H.M.; Gomes, A.R.; Sanders, M.J.; Illingworth, C.J.R.; Billker, O.; Berriman, M.; Lawniczak, M.K. Single-cell RNA-seq reveals hidden transcriptional variation in malaria parasites. eLife, 2018, 7, 7.
[http://dx.doi.org/10.7554/eLife.33105] [PMID: 29580379]
[136]
Walzer, K.A.; Kubicki, D.M.; Tang, X.; Chi, J.T. Single-cell analysis reveals distinct gene expression and heterogeneity in male and female Plasmodium falciparum Gametocytes. MSphere, 2018, 3(2), e00130-e18.
[http://dx.doi.org/10.1128/mSphere.00130-18] [PMID: 29643077]
[137]
Mantel, P.Y.; Hoang, A.N.; Goldowitz, I.; Potashnikova, D.; Hamza, B.; Vorobjev, I.; Ghiran, I.; Toner, M.; Irimia, D.; Ivanov, A.R.; Barteneva, N.; Marti, M. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe, 2013, 13(5), 521-534.
[http://dx.doi.org/10.1016/j.chom.2013.04.009] [PMID: 23684304]
[138]
Baker, D.A. Cyclic nucleotide signalling in malaria parasites. Cell. Microbiol., 2011, 13(3), 331-339.
[http://dx.doi.org/10.1111/j.1462-5822.2010.01561.x] [PMID: 21176056]
[139]
Koyama, F.C.; Chakrabarti, D.; Garcia, C.R. Molecular machinery of signal transduction and cell cycle regulation in Plasmodium. Mol. Biochem. Parasitol., 2009, 165(1), 1-7.
[http://dx.doi.org/10.1016/j.molbiopara.2009.01.003] [PMID: 19393157]
[140]
Cruz, L.N.; Juliano, M.A.; Budu, A.; Juliano, L.; Holder, A.A.; Blackman, M.J.; Garcia, C.R. Extracellular ATP triggers proteolysis and cytosolic Ca2+ rise in Plasmodium berghei and Plasmodium yoelii malaria parasites. Malar. J., 2012, 11(1), 69.
[http://dx.doi.org/10.1186/1475-2875-11-69] [PMID: 22420332]
[141]
Hotta, C.T.; Gazarini, M.L.; Beraldo, F.H.; Varotti, F.P.; Lopes, C.; Markus, R.P.; Pozzan, T.; Garcia, C.R. Calcium-dependent modulation by melatonin of the circadian rhythm in malarial parasites. Nat. Cell Biol., 2000, 2(7), 466-468.
[http://dx.doi.org/10.1038/35017112] [PMID: 10878815]
[142]
Lima, W.R.; Tessarin-Almeida, G.; Rozanski, A.; Parreira, K.S.; Moraes, M.S.; Martins, D.C.; Hashimoto, R.F.; Galante, P.A.F.; Garcia, C.R.S. Signaling transcript profile of the asexual intraerythrocytic development cycle of Plasmodium falciparum induced by melatonin and cAMP. Genes Cancer, 2016, 7(9-10), 323-339.
[http://dx.doi.org/10.18632/genesandcancer.118] [PMID: 28050233]
[143]
Moon, R.W.; Taylor, C.J.; Bex, C.; Schepers, R.; Goulding, D.; Janse, C.J.; Waters, A.P.; Baker, D.A.; Billker, O. A cyclic GMP signalling module that regulates gliding motility in a malaria parasite. PLoS Pathog., 2009, 5(9), e1000599.
[http://dx.doi.org/10.1371/journal.ppat.1000599] [PMID: 19779564]
[144]
Dorin-Semblat, D.; Quashie, N.; Halbert, J.; Sicard, A.; Doerig, C.; Peat, E.; Ranford-Cartwright, L.; Doerig, C. Functional characterization of both MAP kinases of the human malaria parasite Plasmodium falciparum by reverse genetics. Mol. Microbiol., 2007, 65(5), 1170-1180.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05859.x] [PMID: 17651389]
[145]
Madeira, L.; DeMarco, R.; Gazarini, M.L.; Verjovski-Almeida, S.; Garcia, C.R. Human malaria parasites display a receptor for activated C kinase ortholog. Biochem. Biophys. Res. Commun., 2003, 306(4), 995-1001.
[http://dx.doi.org/10.1016/S0006-291X(03)01074-X] [PMID: 12821141]
[146]
Moraes, M.S.; Budu, A.; Singh, M.K.; Borges-Pereira, L.; Levano-Garcia, J.; Currà, C.; Picci, L.; Pace, T.; Ponzi, M.; Pozzan, T.; Garcia, C.R.S. Plasmodium falciparum GPCR-like receptor SR25 mediates extracellular K+ sensing coupled to Ca2+ signaling and stress survival. Sci. Rep., 2017, 7(1), 9545.
[http://dx.doi.org/10.1038/s41598-017-09959-8] [PMID: 28842684]
[147]
Doerig, C.; Baker, D.; Billker, O.; Blackman, M.J.; Chitnis, C.; Dhar Kumar, S.; Heussler, V.; Holder, A.A.; Kocken, C.; Krishna, S.; Langsley, G.; Lasonder, E.; Menard, R.; Meissner, M.; Pradel, G.; Ranford-Cartwright, L.; Sharma, A.; Sharma, P.; Tardieux, T.; Tatu, U.; Alano, P. Signalling in malaria parasites. The MALSIG consortium. Parasite, 2009, 16(3), 169-182.
[http://dx.doi.org/10.1051/parasite/2009163169] [PMID: 19839262]
[148]
Doerig, C.; Rayner, J.C.; Scherf, A.; Tobin, A.B. Post-translational protein modifications in malaria parasites. Nat. Rev. Microbiol., 2015, 13(3), 160-172.
[http://dx.doi.org/10.1038/nrmicro3402] [PMID: 25659318]
[149]
Lima, W.R.; Moraes, M.; Alves, E.; Azevedo, M.F.; Passos, D.O.; Garcia, C.R. The PfNF-YB transcription factor is a downstream target of melatonin and cAMP signalling in the human malaria parasite Plasmodium falciparum. J. Pineal Res., 2013, 54(2), 145-153.
[http://dx.doi.org/10.1111/j.1600-079X.2012.01021.x] [PMID: 22804732]
[150]
Mota, M.M.; Hafalla, J.C.; Rodriguez, A. Migration through host cells activates Plasmodium sporozoites for infection. Nat. Med., 2002, 8(11), 1318-1322.
[http://dx.doi.org/10.1038/nm785] [PMID: 12379848]
[151]
Alexander, D.L.; Arastu-Kapur, S.; Dubremetz, J.F.; Boothroyd, J.C. Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryot. Cell, 2006, 5(7), 1169-1173.
[http://dx.doi.org/10.1128/EC.00040-06] [PMID: 16835460]
[152]
Treeck, M.; Zacherl, S.; Herrmann, S.; Cabrera, A.; Kono, M.; Struck, N.S.; Engelberg, K.; Haase, S.; Frischknecht, F.; Miura, K.; Spielmann, T.; Gilberger, T.W. Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process. PLoS Pathog., 2009, 5(3), e1000322.
[http://dx.doi.org/10.1371/journal.ppat.1000322] [PMID: 19283086]
[153]
Dawn, A.; Singh, S.; More, K.R.; Siddiqui, F.A.; Pachikara, N.; Ramdani, G.; Langsley, G.; Chitnis, C.E. The central role of cAMP in regulating Plasmodium falciparum merozoite invasion of human erythrocytes. PLoS Pathog., 2014, 10(12), e1004520.
[http://dx.doi.org/10.1371/journal.ppat.1004520] [PMID: 25522250]
[154]
Ono, T.; Cabrita-Santos, L.; Leitao, R.; Bettiol, E.; Purcell, L.A.; Diaz-Pulido, O.; Andrews, L.B.; Tadakuma, T.; Bhanot, P.; Mota, M.M.; Rodriguez, A. Adenylyl cyclase alpha and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. PLoS Pathog., 2008, 4(2), e1000008.
[http://dx.doi.org/10.1371/journal.ppat.1000008] [PMID: 18389080]
[155]
Enserink, J.M.; Christensen, A.E.; de Rooij, J.; van Triest, M.; Schwede, F.; Genieser, H.G.; Døskeland, S.O.; Blank, J.L.; Bos, J.L. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol., 2002, 4(11), 901-906.
[http://dx.doi.org/10.1038/ncb874] [PMID: 12402047]
[156]
Gloerich, M.; Bos, J.L. Epac: Defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol., 2010, 50(1), 355-375.
[http://dx.doi.org/10.1146/annurev.pharmtox.010909.105714] [PMID: 20055708]
[157]
Cruz, L.N.; Wu, Y.; Ulrich, H.; Craig, A.G.; Garcia, C.R. Tumor necrosis factor reduces Plasmodium falciparum growth and activates calcium signaling in human malaria parasites. Biochim. Biophys. Acta, 2016, 1860(7), 1489-1497.
[http://dx.doi.org/10.1016/j.bbagen.2016.04.003] [PMID: 27080559]
[158]
Gazarini, M.L.; Beraldo, F.H.; Almeida, F.M.; Bootman, M.; Da Silva, A.M.; Garcia, C.R. Melatonin triggers PKA activation in the rodent malaria parasite Plasmodium chabaudi. J. Pineal Res., 2011, 50(1), 64-70.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00810.x] [PMID: 20964707]
[159]
Cruz, L.N.; Guerra, M.T.; Kruglov, E.; Mennone, A.; Garcia, C.R.; Chen, J.; Nathanson, M.H. Regulation of multidrug resistance-associated protein 2 by calcium signaling in mouse liver. Hepatology, 2010, 52(1), 327-337.
[http://dx.doi.org/10.1002/hep.23625] [PMID: 20578149]
[160]
Alves, E.; Bartlett, P.J.; Garcia, C.R.; Thomas, A.P. Melatonin and IP3-induced Ca2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. J. Biol. Chem., 2011, 286(7), 5905-5912.
[http://dx.doi.org/10.1074/jbc.M110.188474] [PMID: 21149448]
[161]
Beraldo, F.H.; Garcia, C.R. Products of tryptophan catabolism induce Ca2+ release and modulate the cell cycle of Plasmodium falciparum malaria parasites. J. Pineal Res., 2005, 39(3), 224-230.
[http://dx.doi.org/10.1111/j.1600-079X.2005.00249.x] [PMID: 16150101]
[162]
Koyama, F.C.; Carvalho, T.L.; Alves, E.; da Silva, H.B.; de Azevedo, M.F.; Hemerly, A.S.; Garcia, C.R. The structurally related auxin and melatonin tryptophan-derivatives and their roles in Arabidopsis thaliana and in the human malaria parasite Plasmodium falciparum. J. Eukaryot. Microbiol., 2013, 60(6), 646-651.
[http://dx.doi.org/10.1111/jeu.12080] [PMID: 24102716]
[163]
Adjalley, S.H.; Scanfeld, D.; Kozlowski, E.; Llinás, M.; Fidock, D.A. Genome-wide transcriptome profiling reveals functional networks involving the Plasmodium falciparum drug resistance transporters PfCRT and PfMDR1. BMC Genomics, 2015, 16(1), 1090.
[http://dx.doi.org/10.1186/s12864-015-2320-8] [PMID: 26689807]
[164]
Hu, G.; Cabrera, A.; Kono, M.; Mok, S.; Chaal, B.K.; Haase, S.; Engelberg, K.; Cheemadan, S.; Spielmann, T.; Preiser, P.R.; Gilberger, T.W.; Bozdech, Z. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat. Biotechnol., 2010, 28(1), 91-98.
[http://dx.doi.org/10.1038/nbt.1597] [PMID: 20037583]

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