Skip to main content
Top
Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Review

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

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

Published in: Malaria Journal | Issue 1/2018

Login to get access

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.
Literature
1.
go back to reference 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):33–6.PubMedPubMedCentral 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):33–6.PubMedPubMedCentral
2.
go back to reference Haynes JD, Diggs CL, Hines FA, Desjardins RE. Culture of human malaria parasites Plasmodium falciparum. Nature. 1976;263:767–9.CrossRefPubMed Haynes JD, Diggs CL, Hines FA, Desjardins RE. Culture of human malaria parasites Plasmodium falciparum. Nature. 1976;263:767–9.CrossRefPubMed
3.
go back to reference Trager W. A new method for intraerythrocytic cultivation of malaria parasites (Plasmodium coatneyi and P. falciparum). J Protozool. 1971;18:239–42.CrossRefPubMed Trager W. A new method for intraerythrocytic cultivation of malaria parasites (Plasmodium coatneyi and P. falciparum). J Protozool. 1971;18:239–42.CrossRefPubMed
4.
5.
6.
go back to reference WHO. World malaria report. Geneva. World Health Organization. 2015;2015:2–3. WHO. World malaria report. Geneva. World Health Organization. 2015;2015:2–3.
7.
go back to reference Golenda CF, Li J, Rosenberg R. Continuous in vitro propagation of the malaria parasite Plasmodium vivax. Proc Natl Acad Sci USA. 1997;94:6786–91.CrossRefPubMed Golenda CF, Li J, Rosenberg R. Continuous in vitro propagation of the malaria parasite Plasmodium vivax. Proc Natl Acad Sci USA. 1997;94:6786–91.CrossRefPubMed
8.
go back to reference Larrouy G, Magnaval JF, Moro F. Obtaining intraerythrocytic forms of Plasmodium vivax by in vitro culture. C R Seances Acad Sci. 1981;III(292):929–30. Larrouy G, Magnaval JF, Moro F. Obtaining intraerythrocytic forms of Plasmodium vivax by in vitro culture. C R Seances Acad Sci. 1981;III(292):929–30.
9.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
10.
go back to reference 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;37:1551–7.CrossRefPubMed 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;37:1551–7.CrossRefPubMed
11.
go back to reference 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:e74–81.CrossRefPubMedPubMedCentral 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:e74–81.CrossRefPubMedPubMedCentral
12.
go back to reference 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;56:65–9.CrossRefPubMed 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;56:65–9.CrossRefPubMed
13.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
14.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
15.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
16.
go back to reference Moreno-Perez DA, Ruiz JA, Patarroyo MA. Reticulocytes: Plasmodium vivax target cells. Biol Cell. 2013;105:251–60.CrossRefPubMed Moreno-Perez DA, Ruiz JA, Patarroyo MA. Reticulocytes: Plasmodium vivax target cells. Biol Cell. 2013;105:251–60.CrossRefPubMed
17.
go back to reference Furuya T, Sa JM, Chitnis CE, Wellems TE, Stedman TT. Reticulocytes from cryopreserved erythroblasts support Plasmodium vivax infection in vitro. Parasitol Int. 2014;63:278–84.CrossRefPubMed Furuya T, Sa JM, Chitnis CE, Wellems TE, Stedman TT. Reticulocytes from cryopreserved erythroblasts support Plasmodium vivax infection in vitro. Parasitol Int. 2014;63:278–84.CrossRefPubMed
18.
go back to reference 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;42:155–60.CrossRefPubMed 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;42:155–60.CrossRefPubMed
19.
go back to reference 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;3:1314–25.CrossRefPubMed 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;3:1314–25.CrossRefPubMed
20.
go back to reference 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;105:16290–5.CrossRefPubMed 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;105:16290–5.CrossRefPubMed
21.
go back to reference 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;455:757–63.CrossRefPubMedPubMedCentral 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;455:757–63.CrossRefPubMedPubMedCentral
22.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference 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;419:537–42.CrossRefPubMed 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;419:537–42.CrossRefPubMed
25.
26.
go back to reference Wahlgren M, Goel S, Akhouri RR. Variant surface antigens of Plasmodium falciparum and their roles in severe malaria. Nat Rev Microbiol. 2017;15:479–91.CrossRefPubMed Wahlgren M, Goel S, Akhouri RR. Variant surface antigens of Plasmodium falciparum and their roles in severe malaria. Nat Rev Microbiol. 2017;15:479–91.CrossRefPubMed
27.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
29.
go back to reference Cheng Y, Lu F, Tsuboi T, Han ET. Characterization of a novel merozoite surface protein of Plasmodium vivax, Pv41. Acta Trop. 2013;126:222–8.CrossRefPubMed Cheng Y, Lu F, Tsuboi T, Han ET. Characterization of a novel merozoite surface protein of Plasmodium vivax, Pv41. Acta Trop. 2013;126:222–8.CrossRefPubMed
30.
go back to reference 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;54:385–91.CrossRefPubMedPubMedCentral 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;54:385–91.CrossRefPubMedPubMedCentral
31.
go back to reference 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;61:443–9.CrossRefPubMed 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;61:443–9.CrossRefPubMed
32.
go back to reference 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;73:536–40.CrossRefPubMed 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;73:536–40.CrossRefPubMed
33.
go back to reference 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;21:3930–7.CrossRefPubMed 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;21:3930–7.CrossRefPubMed
34.
go back to reference 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;85:672–7.CrossRefPubMed 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;85:672–7.CrossRefPubMed
35.
go back to reference 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;87:1398–403.CrossRefPubMed 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;87:1398–403.CrossRefPubMed
36.
go back to reference 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;478:1211–6.CrossRefPubMed 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;478:1211–6.CrossRefPubMed
37.
go back to reference 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;292:462–76.CrossRefPubMed 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;292:462–76.CrossRefPubMed
38.
go back to reference 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;590:232–41.CrossRefPubMed 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;590:232–41.CrossRefPubMed
39.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
40.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
41.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
42.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
43.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
44.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
45.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
46.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
47.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
48.
go back to reference 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;23:2265–77.CrossRefPubMed 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;23:2265–77.CrossRefPubMed
49.
go back to reference 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;20:1331–9.CrossRefPubMed 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;20:1331–9.CrossRefPubMed
50.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
51.
go back to reference 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. 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.
52.
go back to reference Craig CF. The estivo autumnal (Remittent) malarial fevers. Horace McFarland Company. 1901. Craig CF. The estivo autumnal (Remittent) malarial fevers. Horace McFarland Company. 1901.
53.
54.
go back to reference 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;7:153–64.CrossRef 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;7:153–64.CrossRef
55.
go back to reference Trager W, Jensen JB. Cultivation of erythrocytic stages. Bull World Health Organ. 1977;55:363–5.PubMed Trager W, Jensen JB. Cultivation of erythrocytic stages. Bull World Health Organ. 1977;55:363–5.PubMed
56.
go back to reference Lanners HN. Prolonged in vitro cultivation of Plasmodium vivax using Trager’s continuous-flow method. Parasitol Res. 1992;78:699–701.CrossRefPubMed Lanners HN. Prolonged in vitro cultivation of Plasmodium vivax using Trager’s continuous-flow method. Parasitol Res. 1992;78:699–701.CrossRefPubMed
57.
go back to reference Siddiqui W. In vitro cultivation of Plasmodium vivax and Plasmodium malariae. Cambridge: Adacemic Press; 1979. p. 279–85. Siddiqui W. In vitro cultivation of Plasmodium vivax and Plasmodium malariae. Cambridge: Adacemic Press; 1979. p. 279–85.
58.
go back to reference Brockelman CR, Tan-Ariya P, Laovanitch R. Observation on complete schizogony of Plasmodium vivax in vitro. J Protozool. 1985;32:76–80.CrossRefPubMed Brockelman CR, Tan-Ariya P, Laovanitch R. Observation on complete schizogony of Plasmodium vivax in vitro. J Protozool. 1985;32:76–80.CrossRefPubMed
59.
go back to reference Brockelman C, Laovanitch R, Kaewkes S. Supportive effects of magnesium chloride on viability of Plasmodium vivax in vitro. J Sci Soc Thailand. 1984;10:109–18.CrossRef Brockelman C, Laovanitch R, Kaewkes S. Supportive effects of magnesium chloride on viability of Plasmodium vivax in vitro. J Sci Soc Thailand. 1984;10:109–18.CrossRef
60.
go back to reference 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;18:307–11.CrossRefPubMed 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;18:307–11.CrossRefPubMed
61.
go back to reference 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;66:183–8.CrossRefPubMed 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;66:183–8.CrossRefPubMed
62.
go back to reference 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;169:1795–802.CrossRefPubMed 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;169:1795–802.CrossRefPubMed
63.
go back to reference Sutar NK, Renapurkar DM. Effect of liver extract on growth of Plasmodium vivax in vitro. Indian J Exp Biol. 1991;29:286–7.PubMed Sutar NK, Renapurkar DM. Effect of liver extract on growth of Plasmodium vivax in vitro. Indian J Exp Biol. 1991;29:286–7.PubMed
64.
go back to reference 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;9:258–60.PubMed 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;9:258–60.PubMed
65.
go back to reference 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;95:677–80.CrossRefPubMed 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;95:677–80.CrossRefPubMed
66.
go back to reference 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;108:801–3.CrossRefPubMedPubMedCentral 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;108:801–3.CrossRefPubMedPubMedCentral
67.
go back to reference 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.CrossRef 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.CrossRef
68.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
69.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
70.
go back to reference 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;166:776–85.CrossRefPubMed 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;166:776–85.CrossRefPubMed
71.
go back to reference Pasvol G, Weatherall DJ, Wilson RJ. Effects of foetal haemoglobin on susceptibility of red cells to Plasmodium falciparum. Nature. 1977;270:171–3.CrossRefPubMed Pasvol G, Weatherall DJ, Wilson RJ. Effects of foetal haemoglobin on susceptibility of red cells to Plasmodium falciparum. Nature. 1977;270:171–3.CrossRefPubMed
72.
go back to reference Pasvol G, Weatherall DJ, Wilson RJ, Smith DH, Gilles HM. Fetal haemoglobin and malaria. Lancet. 1976;1:1269–72.CrossRefPubMed Pasvol G, Weatherall DJ, Wilson RJ, Smith DH, Gilles HM. Fetal haemoglobin and malaria. Lancet. 1976;1:1269–72.CrossRefPubMed
73.
go back to reference Heilmeyer LWR. Reifungsstadien an Überlebenden Reticulozyten in vitro und ihre Bedeutung für die Schaetzung der täglichen Haemoglobin-Produktion in vivo. Ztschr Klin Med. 1932;121:361–79. Heilmeyer LWR. Reifungsstadien an Überlebenden Reticulozyten in vitro und ihre Bedeutung für die Schaetzung der täglichen Haemoglobin-Produktion in vivo. Ztschr Klin Med. 1932;121:361–79.
75.
go back to reference 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;15:1938–46.CrossRefPubMedPubMedCentral 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;15:1938–46.CrossRefPubMedPubMedCentral
76.
go back to reference 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;180:118–33.CrossRefPubMed 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;180:118–33.CrossRefPubMed
77.
go back to reference 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;119:6296–306.CrossRefPubMedPubMedCentral 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;119:6296–306.CrossRefPubMedPubMedCentral
78.
go back to reference Koury MJ, Koury ST, Kopsombut P, Bondurant MC. In vitro maturation of nascent reticulocytes to erythrocytes. Blood. 2005;105:2168–74.CrossRefPubMed Koury MJ, Koury ST, Kopsombut P, Bondurant MC. In vitro maturation of nascent reticulocytes to erythrocytes. Blood. 2005;105:2168–74.CrossRefPubMed
79.
go back to reference 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;125:1314–24.CrossRefPubMedPubMedCentral 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;125:1314–24.CrossRefPubMedPubMedCentral
80.
go back to reference Vryonis G. Observations on the parasitization of erythrocytes by Plasmodium vivax, with special reference to reticulocytes. Am J Epidemiol. 1939;30:41–8.CrossRef Vryonis G. Observations on the parasitization of erythrocytes by Plasmodium vivax, with special reference to reticulocytes. Am J Epidemiol. 1939;30:41–8.CrossRef
81.
82.
go back to reference 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;130:1441–4.CrossRefPubMedPubMedCentral 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;130:1441–4.CrossRefPubMedPubMedCentral
83.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
84.
go back to reference 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;108:20113–8.CrossRefPubMed 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;108:20113–8.CrossRefPubMed
85.
go back to reference 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;113:6271–6.CrossRefPubMed 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;113:6271–6.CrossRefPubMed
86.
go back to reference Dubin IN. Bodies suggesting exoerythrocytic forms of Plasmodium vivax in tissue culture. Proc Soc Exp Biol Med. 1947;65:154–6.CrossRefPubMed Dubin IN. Bodies suggesting exoerythrocytic forms of Plasmodium vivax in tissue culture. Proc Soc Exp Biol Med. 1947;65:154–6.CrossRefPubMed
87.
go back to reference Devi C, Pillai C, Subbarao S, Dwivedi SC. Short term in vitro cultivation of erythrocytic stages of Plasmodium vivax. J Parasit Dis. 2000;24:61–6. Devi C, Pillai C, Subbarao S, Dwivedi SC. Short term in vitro cultivation of erythrocytic stages of Plasmodium vivax. J Parasit Dis. 2000;24:61–6.
Metadata
Title
Plasmodium vivax in vitro continuous culture: the spoke in the wheel
Authors
Maritza Bermúdez
Darwin Andrés Moreno-Pérez
Gabriela Arévalo-Pinzón
Hernando Curtidor
Manuel Alfonso Patarroyo
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2456-5

Other articles of this Issue 1/2018

Malaria Journal 1/2018 Go to the issue