Plasmodium vivax in vitro continuous culture: the spoke in the wheel

Maritza Bermúdez, Darwin Andrés Moreno-Pérez, Gabriela Arévalo-Pinzón, Hernando Curtidor, Manuel Alfonso Patarroyo, Maritza Bermúdez, Darwin Andrés Moreno-Pérez, Gabriela Arévalo-Pinzón, Hernando Curtidor, Manuel Alfonso Patarroyo

Abstract

Understanding the life cycle of Plasmodium vivax is fundamental for developing strategies aimed at controlling and eliminating this parasitic species. Although advances in omic sciences and high-throughput techniques in recent years have enabled the identification and characterization of proteins which might be participating in P. vivax invasion of target cells, exclusive parasite tropism for invading reticulocytes has become the main obstacle in maintaining a continuous culture for this species. Such advance that would help in defining each parasite protein's function in the complex process of P. vivax invasion, in addition to evaluating new therapeutic agents, is still a dream. Advances related to maintenance, culture medium supplements and the use of different sources of reticulocytes and parasites (strains and isolates) have been made regarding the development of an in vitro culture for P. vivax; however, only some cultures having few replication cycles have been obtained to date, meaning that this parasite's maintenance goes beyond the technical components involved. Although it is still not yet clear which molecular mechanisms P. vivax prefers for invading young CD71+ reticulocytes [early maturation stages (I-II-III)], changes related to membrane proteins remodelling of such cells could form part of the explanation. The most relevant aspects regarding P. vivax in vitro culture and host cell characteristics have been analysed in this review to explain possible reasons why the species' continuous in vitro culture is so difficult to standardize. Some alternatives for P. vivax in vitro culture have also been described.

Keywords: In vitro culture; Ligand; Plasmodium vivax; Receptor; Reticulocyte.

Figures

Fig. 1
Fig. 1
Plasmodium vivax and P. falciparum merozoite host cell adhesion proteins. The figure shows the P. vivax (left-hand side) and P. falciparum (right-hand side) proteins described to date having a binding-related function regarding receptors identified on target cells: reticulocyte and mature erythrocytes, respectively. Mrz proteins’ subcellular localization is indicated. An asterisk indicates those molecules with unknown subcellular localization
Fig. 2
Fig. 2
Conditions evaluated for culturing Plasmodium vivax in vitro. The figure shows modifications made to culture medium, parasite sources and the target cells which have been used in culturing the P. vivax parasite. Each combination evaluated is described in the culture medium section. For example, 14 indicates RPMI 1640 medium, which contains HEPES, NaHCO3, neomycin, vitamin B12, hypoxanthine, ascorbic acid, MgCl2, biotin, choline and 15% AB+ human serum (box showing typology). The reticulocyte source section lists these cells’ enrichment methodology using the letters a–e. Sections of the graphic enclosed by a red discontinuous line indicate the best target cell sources and/or enrichment methods available so far

References

    1. Brackett RG, Cole GC, Green TJ, Jacobs RL. In vitro propagation of Plasmodium falciparum for merozoite antigens. Bull World Health Organ. 1979;57(Suppl 1):33–36.
    1. Haynes JD, Diggs CL, Hines FA, Desjardins RE. Culture of human malaria parasites Plasmodium falciparum. Nature. 1976;263:767–769. doi: 10.1038/263767a0.
    1. Trager W. A new method for intraerythrocytic cultivation of malaria parasites (Plasmodium coatneyi and P. falciparum) J Protozool. 1971;18:239–242. doi: 10.1111/j.1550-7408.1971.tb03314.x.
    1. Trager W, Jensen JB. Human malaria parasites in continuous culture. Science. 1976;193:673–675. doi: 10.1126/science.781840.
    1. Schwartz L, Brown GV, Genton B, Moorthy VS. A review of malaria vaccine clinical projects based on the WHO rainbow table. Malar J. 2012;11:11. doi: 10.1186/1475-2875-11-11.
    1. WHO. World malaria report Geneva. World Health Organization. 2015;2015:2–3.
    1. Golenda CF, Li J, Rosenberg R. Continuous in vitro propagation of the malaria parasite Plasmodium vivax. Proc Natl Acad Sci USA. 1997;94:6786–6791. doi: 10.1073/pnas.94.13.6786.
    1. Larrouy G, Magnaval JF, Moro F. Obtaining intraerythrocytic forms of Plasmodium vivax by in vitro culture. C R Seances Acad Sci. 1981;III(292):929–930.
    1. Noulin F, Borlon C, van den Eede P, Boel L, Verfaillie CM, D’Alessandro U, Erhart A. Cryopreserved reticulocytes derived from hematopoietic stem cells can be invaded by cryopreserved Plasmodium vivax isolates. PLoS One. 2012;7:e40798. doi: 10.1371/journal.pone.0040798.
    1. Panichakul T, Sattabongkot J, Chotivanich K, Sirichaisinthop J, Cui L, Udomsangpetch R. Production of erythropoietic cells in vitro for continuous culture of Plasmodium vivax. Int J Parasitol. 2007;37:1551–1557. doi: 10.1016/j.ijpara.2007.05.009.
    1. Russell B, Suwanarusk R, Borlon C, Costa FT, Chu CS, Rijken MJ, et al. A reliable ex vivo invasion assay of human reticulocytes by Plasmodium vivax. Blood. 2011;118:e74–e81. doi: 10.1182/blood-2011-04-348748.
    1. Udomsangpetch R, Somsri S, Panichakul T, Chotivanich K, Sirichaisinthop J, Yang Z, et al. Short-term in vitro culture of field isolates of Plasmodium vivax using umbilical cord blood. Parasitol Int. 2007;56:65–69. doi: 10.1016/j.parint.2006.12.005.
    1. Tantular IS, Pusarawati S, Khin L, Kanbe T, Kimura M, Kido Y, et al. Preservation of wild isolates of human malaria parasites in wet ice and adaptation efficacy to in vitro culture. Trop Med Health. 2012;40:37–45. doi: 10.2149/tmh.2012-07o.
    1. Roobsoong W, Tharinjaroen CS, Rachaphaew N, Chobson P, Schofield L, Cui L, et al. Improvement of culture conditions for long-term in vitro culture of Plasmodium vivax. Malar J. 2015;14:297. doi: 10.1186/s12936-015-0815-z.
    1. Shaw-Saliba K, Thomson-Luque R, Obaldia N, 3rd, Nunez M, Dutary S, Lim C, et al. Insights into an optimization of Plasmodium vivax Sal-1 in vitro culture: the Aotus primate model. PLoS Negl Trop Dis. 2016;10:e0004870. doi: 10.1371/journal.pntd.0004870.
    1. Moreno-Perez DA, Ruiz JA, Patarroyo MA. Reticulocytes: Plasmodium vivax target cells. Biol Cell. 2013;105:251–260. doi: 10.1111/boc.201200093.
    1. Furuya T, Sa JM, Chitnis CE, Wellems TE, Stedman TT. Reticulocytes from cryopreserved erythroblasts support Plasmodium vivax infection in vitro. Parasitol Int. 2014;63:278–284. doi: 10.1016/j.parint.2013.11.011.
    1. Borlon C, Russell B, Sriprawat K, Suwanarusk R, Erhart A, Renia L, et al. Cryopreserved Plasmodium vivax and cord blood reticulocytes can be used for invasion and short term culture. Int J Parasitol. 2012;42:155–160. doi: 10.1016/j.ijpara.2011.10.011.
    1. Acharya P, Pallavi R, Chandran S, Chakravarti H, Middha S, Acharya J, et al. A glimpse into the clinical proteome of human malaria parasites Plasmodium falciparum and Plasmodium vivax. Proteomics Clin Appl. 2009;3:1314–1325. doi: 10.1002/prca.200900090.
    1. Bozdech Z, Mok S, Hu G, Imwong M, Jaidee A, Russell B, et al. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc Natl Acad Sci USA. 2008;105:16290–16295. doi: 10.1073/pnas.0807404105.
    1. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature. 2008;455:757–763. doi: 10.1038/nature07327.
    1. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 2003;1:E5. doi: 10.1371/journal.pbio.0000005.
    1. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002;419:498–511. doi: 10.1038/nature01097.
    1. Lasonder E, Ishihama Y, Andersen JS, Vermunt AM, Pain A, Sauerwein RW, et al. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature. 2002;419:537–542. doi: 10.1038/nature01111.
    1. Cowman AF, Healer J, Marapana D, Marsh K. Malaria: biology and disease. Cell. 2016;167:610–624. doi: 10.1016/j.cell.2016.07.055.
    1. Wahlgren M, Goel S, Akhouri RR. Variant surface antigens of Plasmodium falciparum and their roles in severe malaria. Nat Rev Microbiol. 2017;15:479–491. doi: 10.1038/nrmicro.2017.47.
    1. Weiss GE, Gilson PR, Taechalertpaisarn T, Tham WH, de Jong NW, Harvey KL, et al. Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes. PLoS Pathog. 2015;11:e1004670. doi: 10.1371/journal.ppat.1004670.
    1. Wright GJ, Rayner JC. Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLoS Pathog. 2014;10:e1003943. doi: 10.1371/journal.ppat.1003943.
    1. Cheng Y, Lu F, Tsuboi T, Han ET. Characterization of a novel merozoite surface protein of Plasmodium vivax, Pv41. Acta Trop. 2013;126:222–228. doi: 10.1016/j.actatropica.2013.03.002.
    1. Lee SK, Wang B, Han JH, Nyunt MH, Muh F, Chootong P, et al. Characterization of Pv92, a novel merozoite surface protein of Plasmodium vivax. Korean J Parasitol. 2016;54:385–391. doi: 10.3347/kjp.2016.54.4.385.
    1. Li J, Ito D, Chen JH, Lu F, Cheng Y, Wang B, et al. Pv12, a 6-Cys antigen of Plasmodium vivax, is localized to the merozoite rhoptry. Parasitol Int. 2012;61:443–449. doi: 10.1016/j.parint.2012.02.008.
    1. Collins WE, Skinner JC, Pappaioanou M, Ma NS, Broderson JR, Sutton BB, et al. Infection of Aotus vociferans (karyotype V) monkeys with different strains of Plasmodium vivax. J Parasitol. 1987;73:536–540. doi: 10.2307/3282132.
    1. Pico de Coana Y, Rodriguez J, Guerrero E, Barrero C, Rodriguez R, Mendoza M, et al. A highly infective Plasmodium vivax strain adapted to Aotus monkeys: quantitative haematological and molecular determinations useful for P. vivax malaria vaccine development. Vaccine. 2003;21:3930–3937. doi: 10.1016/S0264-410X(03)00278-0.
    1. Sullivan JS, Morris CL, Richardson BB, Galland GG, Jennings VM, Kendall J, et al. Adaptation of the AMRU-1 strain of Plasmodium vivax to Aotus and Saimiri monkeys and to four species of anopheline mosquitoes. J Parasitol. 1999;85:672–677. doi: 10.2307/3285741.
    1. Sullivan JS, Strobert E, Yang C, Morris CL, Galland GG, Richardson BB, et al. Adaptation of a strain of Plasmodium vivax from India to New World monkeys, chimpanzees, and anopheline mosquitoes. J Parasitol. 2001;87:1398–1403. doi: 10.1645/0022-3395(2001)087[1398:AOASOP];2.
    1. Alam MS, Zeeshan M, Rathore S, Sharma YD. Multiple Plasmodium vivax proteins of Pv-fam-a family interact with human erythrocyte receptor Band 3 and have a role in red cell invasion. Biochem Biophys Res Commun. 2016;478:1211–1216. doi: 10.1016/j.bbrc.2016.08.096.
    1. Rathore S, Dass S, Kandari D, Kaur I, Gupta M, Sharma YD. Basigin Interacts with Plasmodium vivax Tryptophan-rich Antigen PvTRAg38 as a second erythrocyte receptor to promote parasite growth. J Biol Chem. 2017;292:462–476. doi: 10.1074/jbc.M116.744367.
    1. Alam MS, Rathore S, Tyagi RK, Sharma YD. Host-parasite interaction: multiple sites in the Plasmodium vivax tryptophan-rich antigen PvTRAg38 interact with the erythrocyte receptor band 3. FEBS Lett. 2016;590:232–241. doi: 10.1002/1873-3468.12053.
    1. Arevalo-Pinzon G, Bermudez M, Curtidor H, Patarroyo MA. The Plasmodium vivax rhoptry neck protein 5 is expressed in the apical pole of Plasmodium vivax VCG-1 strain schizonts and binds to human reticulocytes. Malar J. 2015;14:106. doi: 10.1186/s12936-015-0619-1.
    1. Han JH, Lee SK, Wang B, Muh F, Nyunt MH, Na S, et al. Identification of a reticulocyte-specific binding domain of Plasmodium vivax reticulocyte-binding protein 1 that is homologous to the PfRh4 erythrocyte-binding domain. Sci Rep. 2016;6:26993. doi: 10.1038/srep26993.
    1. Franca CT, He WQ, Gruszczyk J, Lim NT, Lin E, Kiniboro B, et al. Plasmodium vivax reticulocyte binding proteins are key targets of naturally acquired immunity in young Papua New Guinean children. PLoS Negl Trop Dis. 2016;10:e0005014. doi: 10.1371/journal.pntd.0005014.
    1. Gruszczyk J, Kanjee U, Chan LJ, Menant S, Malleret B, Lim NTY, et al. Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax. Science. 2018;359:48–55. doi: 10.1126/science.aan1078.
    1. Ntumngia FB, Thomson-Luque R, Torres Lde M, Gunalan K, Carvalho LH, Adams JH. A novel erythrocyte binding protein of Plasmodium vivax suggests an alternate invasion pathway into Duffy-positive reticulocytes. MBio. 2016;7:e01261. doi: 10.1128/mBio.01261-16.
    1. Baquero LA, Moreno-Perez DA, Garzon-Ospina D, Forero-Rodriguez J, Ortiz-Suarez HD, Patarroyo MA. PvGAMA reticulocyte binding activity: predicting conserved functional regions by natural selection analysis. Parasit Vectors. 2017;10:251. doi: 10.1186/s13071-017-2183-8.
    1. Moreno-Perez DA, Baquero LA, Chitiva-Ardila DM, Patarroyo MA. Characterising PvRBSA: an exclusive protein from Plasmodium species infecting reticulocytes. Parasit Vectors. 2017;10:243. doi: 10.1186/s13071-017-2185-6.
    1. Batchelor JD, Malpede BM, Omattage NS, DeKoster GT, Henzler-Wildman KA, Tolia NH. Red blood cell invasion by Plasmodium vivax: structural basis for DBP engagement of DARC. PLoS Pathog. 2014;10:e1003869. doi: 10.1371/journal.ppat.1003869.
    1. Ocampo M, Vera R, Eduardo Rodriguez L, Curtidor H, Urquiza M, Suarez J, et al. Plasmodium vivax Duffy binding protein peptides specifically bind to reticulocytes. Peptides. 2002;23:13–22. doi: 10.1016/S0196-9781(01)00574-5.
    1. Urquiza M, Patarroyo MA, Mari V, Ocampo M, Suarez J, Lopez R, et al. Identification and polymorphism of Plasmodium vivax RBP-1 peptides which bind specifically to reticulocytes. Peptides. 2002;23:2265–2277. doi: 10.1016/S0196-9781(02)00267-X.
    1. Rodriguez LE, Urquiza M, Ocampo M, Curtidor H, Suarez J, Garcia J, et al. Plasmodium vivax MSP-1 peptides have high specific binding activity to human reticulocytes. Vaccine. 2002;20:1331–1339. doi: 10.1016/S0264-410X(01)00472-8.
    1. Arevalo-Pinzon G, Bermudez M, Hernandez D, Curtidor H, Patarroyo MA. Plasmodium vivax ligand-receptor interaction: PvAMA-1 domain I contains the minimal regions for specific interaction with CD71+ reticulocytes. Sci Rep. 2017;7:9616. doi: 10.1038/s41598-017-10025-6.
    1. Bermudez M, Arevalo-Pinzon G, Rubio L, Chaloin O, Muller S, Curtidor H, et al. Receptor-ligand and parasite protein-protein interactions in Plasmodium vivax: Analysing rhoptry neck proteins 2 and 4. Cell Microbiol. 2018:e12835.
    1. Craig CF. The estivo autumnal (Remittent) malarial fevers. Horace McFarland Company. 1901.
    1. Bass CC, Johns FM. The cultivation of malarial plasmodia (Plasmodium vivax and Plasmodium falciparum) in vitro. J Exp Med. 1912;16:567–579. doi: 10.1084/jem.16.4.567.
    1. Thomson JG, Thomson D, Fantham HB. The cultivation of one generation of benign tertian malarial parasites (Plasmodium vivax) in vitro, by Bass’s method. Ann Trop Med Parasitol. 1913;7:153–164. doi: 10.1080/00034983.1913.11687607.
    1. Trager W, Jensen JB. Cultivation of erythrocytic stages. Bull World Health Organ. 1977;55:363–365.
    1. Lanners HN. Prolonged in vitro cultivation of Plasmodium vivax using Trager’s continuous-flow method. Parasitol Res. 1992;78:699–701. doi: 10.1007/BF00931524.
    1. Siddiqui W. In vitro cultivation of Plasmodium vivax and Plasmodium malariae. Cambridge: Adacemic Press; 1979. pp. 279–285.
    1. Brockelman CR, Tan-Ariya P, Laovanitch R. Observation on complete schizogony of Plasmodium vivax in vitro. J Protozool. 1985;32:76–80. doi: 10.1111/j.1550-7408.1985.tb03016.x.
    1. Brockelman C, Laovanitch R, Kaewkes S. Supportive effects of magnesium chloride on viability of Plasmodium vivax in vitro. J Sci Soc Thailand. 1984;10:109–118. doi: 10.2306/scienceasia1513-1874.1984.10.109.
    1. Mons B, Croon JJ, van der Star W, van der Kaay HJ. Erythrocytic schizogony and invasion of Plasmodium vivax in vitro. Int J Parasitol. 1988;18:307–311. doi: 10.1016/0020-7519(88)90138-5.
    1. Mons B, Collins WE, Skinner JC, van der Star W, Croon JJ, van der Kaay HJ. Plasmodium vivax: in vitro growth and reinvasion in red blood cells of Aotus nancymai. Exp Parasitol. 1988;66:183–188. doi: 10.1016/0014-4894(88)90089-6.
    1. Barnwell JW, Nichols ME, Rubinstein P. In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med. 1989;169:1795–1802. doi: 10.1084/jem.169.5.1795.
    1. Sutar NK, Renapurkar DM. Effect of liver extract on growth of Plasmodium vivax in vitro. Indian J Exp Biol. 1991;29:286–287.
    1. Zhou WZ, Hu LQ. [Erythrocytic schizogony of Plasmodium vivax under various conditions of in vitro cultivation](in Chinese) Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 1991;9:258–260.
    1. Chotivanich K, Silamut K, Udomsangpetch R, Stepniewska KA, Pukrittayakamee S, Looareesuwan S, et al. Ex-vivo short-term culture and developmental assessment of Plasmodium vivax. Trans R Soc Trop Med Hyg. 2001;95:677–680. doi: 10.1016/S0035-9203(01)90113-0.
    1. Fernandez-Becerra C, Lelievre J, Ferrer M, Anton N, Thomson R, Peligero C, et al. Red blood cells derived from peripheral blood and bone marrow CD34(+) human haematopoietic stem cells are permissive to Plasmodium parasites infection. Mem Inst Oswaldo Cruz. 2013;108:801–803. doi: 10.1590/0074-0276108062013019.
    1. Singh G, Urhekar AD, Singh R. In vitro cultivation of Plasmodium vivax using McCoy’s medium. Asian J Med Pharm Res. 2015;5:18–21. doi: 10.5958/2231-5659.2015.00004.1.
    1. Rangel GW, Clark MA, Kanjee U, Lim C, Shaw-Saliba K, Menezes MJ, et al. Enhanced ex vivo Plasmodium vivax intraerythrocytic enrichment and maturation for rapid and sensitive parasite growth assays. Antimicrob Agents Chemother. 2018;62:e02519. doi: 10.1128/AAC.02519-17.
    1. Mehlotra RK, Blankenship D, Howes RE, Rakotomanga TA, Ramiranirina B, Ramboarina S, et al. Long-term in vitro culture of Plasmodium vivax isolates from Madagascar maintained in Saimiri boliviensis blood. Malar J. 2017;16:442. doi: 10.1186/s12936-017-2090-7.
    1. Nichols ME, Rubinstein P, Barnwell J, de Cordoba RS, Rosenfield RE. A new human Duffy blood group specificity defined by a murine monoclonal antibody Immunogenetics and association with susceptibility to Plasmodium vivax. J Exp Med. 1987;166:776–785. doi: 10.1084/jem.166.3.776.
    1. Pasvol G, Weatherall DJ, Wilson RJ. Effects of foetal haemoglobin on susceptibility of red cells to Plasmodium falciparum. Nature. 1977;270:171–173. doi: 10.1038/270171a0.
    1. Pasvol G, Weatherall DJ, Wilson RJ, Smith DH, Gilles HM. Fetal haemoglobin and malaria. Lancet. 1976;1:1269–1272. doi: 10.1016/S0140-6736(76)91738-4.
    1. Heilmeyer LWR. Reifungsstadien an Überlebenden Reticulozyten in vitro und ihre Bedeutung für die Schaetzung der täglichen Haemoglobin-Produktion in vivo. Ztschr Klin Med. 1932;121:361–379.
    1. Liu J, Guo X, Mohandas N, Chasis JA, An X. Membrane remodeling during reticulocyte maturation. Blood. 2010;115:2021–2027. doi: 10.1182/blood-2009-08-241182.
    1. Wilson MC, Trakarnsanga K, Heesom KJ, Cogan N, Green C, Toye AM, et al. Comparison of the proteome of adult and cord erythroid cells, and changes in the proteome following reticulocyte maturation. Mol Cell Proteomics. 2016;15:1938–1946. doi: 10.1074/mcp.M115.057315.
    1. Chu TTT, Sinha A, Malleret B, Suwanarusk R, Park JE, Naidu R, et al. Quantitative mass spectrometry of human reticulocytes reveal proteome-wide modifications during maturation. Br J Haematol. 2018;180:118–133. doi: 10.1111/bjh.14976.
    1. Griffiths RE, Kupzig S, Cogan N, Mankelow TJ, Betin VM, Trakarnsanga K, et al. Maturing reticulocytes internalize plasma membrane in glycophorin A-containing vesicles that fuse with autophagosomes before exocytosis. Blood. 2012;119:6296–6306. doi: 10.1182/blood-2011-09-376475.
    1. Koury MJ, Koury ST, Kopsombut P, Bondurant MC. In vitro maturation of nascent reticulocytes to erythrocytes. Blood. 2005;105:2168–2174. doi: 10.1182/blood-2004-02-0616.
    1. Malleret B, Li A, Zhang R, Tan KS, Suwanarusk R, Claser C, et al. Plasmodium vivax: restricted tropism and rapid remodeling of CD71-positive reticulocytes. Blood. 2015;125:1314–1324. doi: 10.1182/blood-2014-08-596015.
    1. Vryonis G. Observations on the parasitization of erythrocytes by Plasmodium vivax, with special reference to reticulocytes. Am J Epidemiol. 1939;30:41–48. doi: 10.1093/oxfordjournals.aje.a118587.
    1. Hillman RS. Characteristics of marrow production and reticulocyte maturation in normal man in response to anemia. J Clin Invest. 1969;48:443–453. doi: 10.1172/JCI106001.
    1. Ovchynnikova E, Aglialoro F, Bentlage AEH, Vidarsson G, Salinas ND, von Lindern M, et al. DARC extracellular domain remodeling in maturating reticulocytes explains Plasmodium vivax tropism. Blood. 2017;130:1441–1444. doi: 10.1182/blood-2017-03-774364.
    1. Martin-Jaular L, Elizalde-Torrent A, Thomson-Luque R, Ferrer M, Segovia JC, Herreros-Aviles E, et al. Reticulocyte-prone malaria parasites predominantly invade CD71hi immature cells: implications for the development of an in vitro culture for Plasmodium vivax. Malar J. 2013;12:434. doi: 10.1186/1475-2875-12-434.
    1. King CL, Adams JH, Xianli J, Grimberg BT, McHenry AM, Greenberg LJ, et al. Fy(a)/Fy(b) antigen polymorphism in human erythrocyte Duffy antigen affects susceptibility to Plasmodium vivax malaria. Proc Natl Acad Sci USA. 2011;108:20113–20118. doi: 10.1073/pnas.1109621108.
    1. Gunalan K, Lo E, Hostetler JB, Yewhalaw D, Mu J, Neafsey DE, et al. Role of Plasmodium vivax Duffy-binding protein 1 in invasion of Duffy-null Africans. Proc Natl Acad Sci USA. 2016;113:6271–6276. doi: 10.1073/pnas.1606113113.
    1. Dubin IN. Bodies suggesting exoerythrocytic forms of Plasmodium vivax in tissue culture. Proc Soc Exp Biol Med. 1947;65:154–156. doi: 10.3181/00379727-65-15895.
    1. Devi C, Pillai C, Subbarao S, Dwivedi SC. Short term in vitro cultivation of erythrocytic stages of Plasmodium vivax. J Parasit Dis. 2000;24:61–66.

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