Sistemas de expresión de proteínas recombinantes para el análisis funcional de antígenos de Plasmodium falciparum y Plasmodium vivax: una revisión
Recombinant Protein Expression Systems for Functional Analysis of Plasmodium falciparum and Plasmodium vivax Antigens: A Review
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Introducción: Para diseñar vacunas es necesario comprender la función de los antígenos de Plasmodium spp. involucrados en la invasión a células hospederas. Diferentes investigaciones han generado proteínas recombinantes utilizando sistemas de expresión heterólogos y así han obtenido moléculas semejantes a las nativas. Con estos avances se desarrollan estrategias que bloquean la infección de estos patógenos. Objetivo: Describir las características y los aspectos metodológicos más importantes de los sistemas de expresión de las proteínas recombinantes en estudios funcionales de Plasmodium spp. Metodología: Revisión descriptiva de estudios publicados en Pubmed, Science Direct, Embase y Medline, entre 2010 y 2020, que incluyeran sistemas recombinantes en células de Escherichia coli, de mamífero y sistemas libres de células, para estudios funcionales de antígenos de Plasmodium falciparum y Plasmodium vivax. Se revisaron 70 artículos originales y 58 cumplieron con los criterios establecidos. Resultados: Obtener proteínas recombinantes mediante un sistema procariota, de mayor rendimiento y bajo costo, ha permitido estudiar un número importante de antígenos. Los sistemas con células de mamífero y libres de células, que permiten modificaciones postraduccionales y plegamiento adecuado de moléculas, se usan para producir librerías de antígenos con estructura conformacional similar a la nativa. Conclusión: El estudio de los antígenos de Plasmodium spp. implicados en la infección y desarrollo de células diana requiere una adecuada selección del método de producción recombinante. El refinamiento de procesos de expresión en sistemas procariotas, eucariotas e in vitro, mediante ingeniería genética y cultivo celular, permitirá mejores rendimientos y menor costo.
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Referencias (VER)
World Health Organization. Word Malaria Report 2019. Report. World Health Organization 2019.
Cowman AF, Healer J, Marapana D, Marsh K. Malaria: Biology and Disease. Cell. 2016;167(3):610-24. https://doi.org/10.1016/j.cell.2016.07.055
Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis. 2012;6(9):e1814. https://doi.org/10.1371/journal.pntd.0001814
Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM. Vivax malaria: neglected and not benign. Am J Trop Med Hyg. 2007;77(6 Suppl):79-87. https://doi.org/10.4269/ajtmh.2007.77.79
Venkatesh A, Patel SK, Ray S, Shastri J, Chatterjee G, Kochar SK, et al. Proteomics of Plasmodium vivax malaria: new insights, progress and potential. Expert review of proteomics. 2016;13(8):771-82. https://doi.org/10.1080/14789450.2016.1210515
Moreno-Perez DA, Degano R, Ibarrola N, Muro A, Patarroyo MA. Determining the Plasmodium vivax VCG-1 strain blood stage proteome. J Proteomics. 2015;113:268-80. https://doi.org/10.1016/j.jprot.2014.10.003
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 Clinical applications. 2009;3(11):1314-25. https://doi.org/10.1002/prca.200900090
Boucher MJ, Ghosh S, Zhang L, Lal A, Jang SW, Ju A, et al. Integrative proteomics and bioinformatic prediction enable a high-confidence apicoplast proteome in malaria parasites. PLoS biology. 2018;16(9):e2005895. https://doi.org/10.1371/journal.pbio.2005895
Bunnik EM, Batugedara G, Saraf A, Prudhomme J, Florens L, Le Roch KG. The mRNA-bound proteome of the human malaria parasite Plasmodium falciparum. Genome Biol. 2016;17(1):147. https://doi.org/10.1186/s13059-016-1014-0
Alam MS, Choudhary V, Zeeshan M, Tyagi RK, Rathore S, Sharma YD. Interaction of Plasmodium vivax Tryptophan-rich Antigen PvTRAg38 with Band 3 on Human Erythrocyte Surface Facilitates Parasite Growth. The Journal of biological chemistry. 2015;290(33):20257-72. https://doi.org/10.1074/jbc.M115.644906
Arevalo-Pinzon G, Curtidor H, Patino LC, Patarroyo MA. PvRON2, a new Plasmodium vivax rhoptry neck antigen. Malaria journal. 2011;10:60. https://doi.org/10.1186/1475-2875-10-60
Bartholdson SJ, Bustamante LY, Crosnier C, Johnson S, Lea S, Rayner JC, et al. Semaphorin-7A is an erythrocyte receptor for P. falciparum merozoite-specific TRAP homolog, MTRAP. PLoS pathogens. 2012;8(11):e1003031. https://doi.org/10.1371/journal.ppat.1003031
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 pathogens. 2014;10(1):e1003869. https://doi.org/10.1371/journal.ppat.1003869
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. Cellular microbiology. 2018;20(7):e12835. https://doi.org/10.1111/cmi.12835
Chen Q, Pettersson F, Vogt AM, Schmidt B, Ahuja S, Liljestrom P, et al. Immunization with PfEMP1-DBL1alpha generates antibodies that disrupt rosettes and protect against the sequestration of Plasmodium falciparum-infected erythrocytes. Vaccine. 2004;22(21-22):2701-12. https://doi.org/10.1016/j.vaccine.2004.02.015
Cheng Y, Lu F, Tsuboi T, Han ET. Characterization of a novel merozoite surface protein of Plasmodium vivax, Pv41. Acta tropica. 2013;126(3):222-8. https://doi.org/10.1016/j.actatropica.2013.03.002
Douglas AD, Williams AR, Knuepfer E, Illingworth JJ, Furze JM, Crosnier C, et al. Neutralization of Plasmodium falciparum merozoites by antibodies against PfRH5. J Immunol. 2014;192(1):245-58. https://doi.org/10.4049/jimmunol.1302045
Duraisingh MT, Maier AG, Triglia T, Cowman AF. Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and -independent pathways. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(8):4796-801. https://doi.org/10.1073/pnas.0730883100
Dundas K, Shears MJ, Sun Y, Hopp CS, Crosnier C, Metcalf T, et al. Alpha-v-containing integrins are host receptors for the Plasmodium falciparum sporozoite surface protein, TRAP. Proceedings of the National Academy of Sciences of the United States of America. 2018;115(17):4477-82. https://doi.org/10.1073/pnas.1719660115
Favuzza P, Guffart E, Tamborrini M, Scherer B, Dreyer AM, Rufer AC, et al. Structure of the malaria vaccine candidate antigen CyRPA and its complex with a parasite invasion inhibitory antibody. eLife. 2017;6. https://doi.org/10.7554/eLife.20383
Khattab A, Bonow I, Schreiber N, Petter M, Schmetz C, Klinkert MQ. Plasmodium falciparum variant STEVOR antigens are expressed in merozoites and possibly associated with erythrocyte invasion. Malaria journal. 2008;7:137. https://doi.org/10.1186/1475-2875-7-137
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. The Journal of biological chemistry. 2017;292(2):462-76. https://doi.org/10.1074/jbc.M116.744367
Salamanca DR, Gomez M, Camargo A, Cuy-Chaparro L, Molina-Franky J, Reyes C, et al. Plasmodium falciparum Blood Stage Antimalarial Vaccines: An Analysis of Ongoing Clinical Trials and New Perspectives Related to Synthetic Vaccines. Front Microbiol. 2019;10:2712. https://doi.org/10.3389/fmicb.2019.02712
Alanine DGW, Quinkert D, Kumarasingha R, Mehmood S, Donnellan FR, Minkah NK, et al. Human Antibodies that Slow Erythrocyte Invasion Potentiate Malaria-Neutralizing Antibodies. Cell. 2019;178(1):216-28 e21. https://doi.org/10.1016/j.cell.2019.05.025
Chen L, Xu Y, Wong W, Thompson JK, Healer J, Goddard-Borger ED, et al. Structural basis for inhibition of erythrocyte invasion by antibodies to Plasmodium falciparum protein CyRPA. eLife. 2017;6. https://doi.org/10.7554/eLife.21347
Chootong P, Ntumngia FB, VanBuskirk KM, Xainli J, Cole-Tobian JL, Campbell CO, et al. Mapping epitopes of the Plasmodium vivax Duffy binding protein with naturally acquired inhibitory antibodies. Infection and immunity. 2010;78(3):1089-95. https://doi.org/10.1128/IAI.01036-09
Gao X, Yeo KP, Aw SS, Kuss C, Iyer JK, Genesan S, et al. Antibodies targeting the PfRH1 binding domain inhibit invasion of Plasmodium falciparum merozoites. PLoS pathogens. 2008;4(7):e1000104. https://doi.org/10.1371/journal.ppat.1000104
Healer J, Thompson JK, Riglar DT, Wilson DW, Chiu YH, Miura K, et al. Vaccination with conserved regions of erythrocyte-binding antigens induces neutralizing antibodies against multiple strains of Plasmodium falciparum. PLoS One. 2013;8(9):e72504. https://doi.org/10.1371/journal.pone.0072504
Nicolete VC, Frischmann S, Barbosa S, King CL, Ferreira MU. Naturally Acquired Binding-Inhibitory Antibodies to Plasmodium vivax Duffy Binding Protein and Clinical Immunity to Malaria in Rural Amazonians. J Infect Dis. 2016;214(10):1539-46. https://doi.org/10.1093/infdis/jiw407
Zhou AE, Berry AA, Bailey JA, Pike A, Dara A, Agrawal S, et al. Antibodies to Peptides in Semiconserved Domains of RIFINs and STEVORs Correlate with Malaria Exposure. mSphere. 2019;4(2). https://doi.org/10.1128/mSphere.00097-19
Hostetler JB, Sharma S, Bartholdson SJ, Wright GJ, Fairhurst RM, Rayner JC. A Library of Plasmodium vivax Recombinant Merozoite Proteins Reveals New Vaccine Candidates and Protein-Protein Interactions. PLoS Negl Trop Dis. 2015;9(12):e0004264. https://doi.org/10.1371/journal.pntd.0004264
Draper SJ, Sack BK, King CR, Nielsen CM, Rayner JC, Higgins MK, et al. Malaria Vaccines: Recent Advances and New Horizons. Cell Host Microbe. 2018;24(1):43-56. https://doi.org/10.1016/j.chom.2018.06.008
Singh K, Mukherjee P, Shakri AR, Singh A, Pandey G, Bakshi M, et al. Malaria vaccine candidate based on Duffy-binding protein elicits strain transcending functional antibodies in a Phase I trial. NPJ Vaccines. 2018;3:48. https://doi.org/10.1038/s41541-018-0083-3
Zheng J, Pan H, Gu Y, Zuo X, Ran N, Yuan Y, et al. Prospects for Malaria Vaccines: Pre-Erythrocytic Stages, Blood Stages, and Transmission-Blocking Stages. Biomed Res Int. 2019;2019:9751471. https://doi.org/10.1155/2019/9751471
Yadavalli R, Ledger C, Sam-Yellowe TY. In vitro human cell-free expression system for synthesis of malaria proteins. Parasitol Res. 2012;111(6):2461-5. https://doi.org/10.1007/s00436-012-3014-7
Srivastava A, Durocher Y, Gamain B. Expressing full-length functional PfEMP1 proteins in the HEK293 expression system. Methods Mol Biol. 2013;923:307-19. https://doi.org/10.1007/978-1-62703-026-7_22
Zemella A, Thoring L, Hoffmeister C, Kubick S. Cell-Free Protein Synthesis: Pros and Cons of Prokaryotic and Eukaryotic Systems. Chembiochem. 2015;16(17):2420-31.
https://doi.org/10.1002/cbic.201500340
Hacker DL, Balasubramanian S. Recombinant protein production from stable mammalian cell lines and pools. Curr Opin Struct Biol. 2016;38:129-36. https://doi.org/10.1016/j.sbi.2016.06.005
Wingfield PT. Overview of the purification of recombinant proteins. Curr Protoc Protein Sci. 2015;80:6 1 -6 1 35. https://doi.org/10.1002/0471140864.ps0601s80
Ferrer-Miralles N, Saccardo P, Corchero JL, Xu Z, Garcia-Fruitos E. General introduction: recombinant protein production and purification of insoluble proteins. Methods Mol Biol. 2015;1258:1-24. https://doi.org/10.1007/978-1-4939-2205-5_1
Patarroyo MA, Arevalo-Pinzon G, Moreno-Perez DA. From a basic to a functional approach for developing a blood stage vaccine against Plasmodium vivax. Expert Rev Vaccines. 2020;19(2):195-207. https://doi.org/10.1080/14760584.2020.1733421
Sirima SB, Durier C, Kara L, Houard S, Gansane A, Loulergue P, et al. Safety and immunogenicity of a recombinant Plasmodium falciparum AMA1-DiCo malaria vaccine adjuvanted with GLA-SE or Alhydrogel(R) in European and African adults: A phase 1a/1b, randomized, double-blind multi-centre trial. Vaccine. 2017;35(45):6218-27. https://doi.org/10.1016/j.vaccine.2017.09.027
Gaur D, Singh S, Singh S, Jiang L, Diouf A, Miller LH. Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(45):17789-94. https://doi.org/10.1073/pnas.0708772104
Rosa DS, Iwai LK, Tzelepis F, Bargieri DY, Medeiros MA, Soares IS, et al. Immunogenicity of a recombinant protein containing the Plasmodium vivax vaccine candidate MSP1(19) and two human CD4+ T-cell epitopes administered to non-human primates (Callithrix jacchus jacchus). Microbes Infect. 2006;8(8):2130-7. https://doi.org/10.1016/j.micinf.2006.03.012
Gileadi O. Recombinant Protein Expression in E. coli : A Historical Perspective. Methods Mol Biol. 2017;1586:3-10. https://doi.org/10.1007/978-1-4939-6887-9_1
Gopal GJ, Kumar A. Strategies for the production of recombinant protein in Escherichia coli. Protein J. 2013;32(6):419-25. https://doi.org/10.1007/s10930-013-9502-5
Rosano GL, Morales ES, Ceccarelli EA. New tools for recombinant protein production in Escherichia coli: A 5-year update. Protein Sci. 2019;28(8):1412-22.
https://doi.org/10.1002/pro.3668
Hayat SMG, Farahani N, Golichenari B, Sahebkar A. Recombinant Protein Expression in Escherichia coli (E.coli): What We Need to Know. Curr Pharm Des. 2018;24(6):718-25. https://doi.org/10.2174/1381612824666180131121940
Flick K, Ahuja S, Chene A, Bejarano MT, Chen Q. Optimized expression of Plasmodium falciparum erythrocyte membrane protein 1 domains in Escherichia coli. Malaria journal. 2004;3:50. https://doi.org/10.1186/1475-2875-3-50
Reddy KS, Amlabu E, Pandey AK, Mitra P, Chauhan VS, Gaur D. Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(4):1179-84. https://doi.org/10.1073/pnas.1415466112
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(4). https://doi.org/10.1128/mBio.01261-16
Muh F, Han JH, Nyunt MH, Lee SK, Jeon HY, Ha KS, et al. Identification of a novel merozoite surface antigen of Plasmodium vivax, PvMSA180. Malaria journal. 2017;16(1):133. https://doi.org/10.1186/s12936-017-1760-9
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. Malaria journal. 2015;14:106. https://doi.org/10.1186/s12936-015-0619-1
Arevalo-Pinzon G, Curtidor H, Abril J, Patarroyo MA. Annotation and characterization of the Plasmodium vivax rhoptry neck protein 4 (PvRON4). Malaria journal. 2013;12:356. https://doi.org/10.1186/1475-2875-12-356
Deshmukh A, Chourasia BK, Mehrotra S, Kana IH, Paul G, Panda A, et al. Plasmodium falciparum MSP3 Exists in a Complex on the Merozoite Surface and Generates Antibody Response during Natural Infection. Infection and immunity. 2018;86(8). https://doi.org/10.1128/IAI.00067-18
Sisquella X, Nebl T, Thompson JK, Whitehead L, Malpede BM, Salinas ND, et al. Plasmodium falciparum ligand binding to erythrocytes induce alterations in deformability essential for invasion. eLife. 2017;6. https://doi.org/10.7554/eLife.21083
Gupta ED, Anand G, Singh H, Chaddha K, Bharti PK, Singh N, et al. Naturally Acquired Human Antibodies Against Reticulocyte-Binding Domains of Plasmodium vivax Proteins, PvRBP2c and PvRBP1a, Exhibit Binding-Inhibitory Activity. J Infect Dis. 2017;215(10):1558-68. https://doi.org/10.1093/infdis/jix170
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(1):9616.
https://doi.org/10.1038/s41598-017-10025-6
Chen S, Gray D, Ma J, Subramanian S. Production of recombinant proteins in mammalian cells. Curr Protoc Protein Sci. 2001;Chapter 5:Unit5 10.
Bandaranayake AD, Almo SC. Recent advances in mammalian protein production. FEBS letters. 2014;588(2):253-60. https://doi.org/10.1016/j.febslet.2013.11.035
O'Flaherty R, Bergin A, Flampouri E, Mota LM, Obaidi I, Quigley A, et al. Mammalian cell culture for production of recombinant proteins: A review of the critical steps in their biomanufacturing. Biotechnol Adv. 2020:107552. https://doi.org/10.1016/j.biotechadv.2020.107552
Crosnier C, Wanaguru M, McDade B, Osier FH, Marsh K, Rayner JC, et al. A library of functional recombinant cell-surface and secreted P. falciparum merozoite proteins. Mol Cell Proteomics. 2013;12(12):3976-86. https://doi.org/10.1074/mcp.O113.028357
Zenonos ZA, Rayner JC, Wright GJ. Towards a comprehensive Plasmodium falciparum merozoite cell surface and secreted recombinant protein library. Malaria journal. 2014;13:93. https://doi.org/10.1186/1475-2875-13-93
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(9):e0005014. https://doi.org/10.1371/journal.pntd.0005014
Franca CT, White MT, He WQ, Hostetler JB, Brewster J, Frato G, et al. Identification of highly-protective combinations of Plasmodium vivax recombinant proteins for vaccine development. eLife. 2017;6. https://doi.org/10.7554/eLife.28673
Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M, Uchikawa M, et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature. 2011;480(7378):534-7. https://doi.org/10.1038/nature10606
Rodriguez M, Lustigman S, Montero E, Oksov Y, Lobo CA. PfRH5: a novel reticulocyte-binding family homolog of plasmodium falciparum that binds to the erythrocyte, and an investigation of its receptor. PLoS One. 2008;3(10):e3300. https://doi.org/10.1371/journal.pone.0003300
Arevalo-Pinzon G, Curtidor H, Munoz M, Patarroyo MA, Bermudez A, Patarroyo ME. A single amino acid change in the Plasmodium falciparum RH5 (PfRH5) human RBC binding sequence modifies its structure and determines species-specific binding activity. Vaccine. 2012;30(3):637-46. https://doi.org/10.1016/j.vaccine.2011.11.012
Wanaguru M, Crosnier C, Johnson S, Rayner JC, Wright GJ. Biochemical analysis of the Plasmodium falciparum erythrocyte-binding antigen-175 (EBA175)-glycophorin-A interaction: implications for vaccine design. The Journal of biological chemistry. 2013;288(45):32106-17. https://doi.org/10.1074/jbc.M113.484840
Tamborrini M, Hauser J, Schafer A, Amacker M, Favuzza P, Kyungtak K, et al. Vaccination with virosomally formulated recombinant CyRPA elicits protective antibodies against Plasmodium falciparum parasites in preclinical in vitro and in vivo models. NPJ Vaccines. 2020;5:9. https://doi.org/10.1038/s41541-020-0158-9
Morita M, Takashima E, Ito D, Miura K, Thongkukiatkul A, Diouf A, et al. Immunoscreening of Plasmodium falciparum proteins expressed in a wheat germ cell-free system reveals a novel malaria vaccine candidate. Sci Rep. 2017;7:46086. https://doi.org/10.1038/srep46086
Kanoi BN, Takashima E, Morita M, White MT, Palacpac NM, Ntege EH, et al. Antibody profiles to wheat germ cell-free system synthesized Plasmodium falciparum proteins correlate with protection from symptomatic malaria in Uganda. Vaccine. 2017;35(6):873-81. https://doi.org/10.1016/j.vaccine.2017.01.001
Takeda M, Kainosho M. Cell-free protein production for NMR studies. Methods Mol Biol. 2012;831:71-84. https://doi.org/10.1007/978-1-61779-480-3_5
Tsuboi T, Takeo S, Iriko H, Jin L, Tsuchimochi M, Matsuda S, et al. Wheat germ cell-free system-based production of malaria proteins for discovery of novel vaccine candidates. Infection and immunity. 2008;76(4):1702-8. https://doi.org/10.1128/IAI.01539-07
Yadavalli R, Sam-Yellowe T. HeLa Based Cell Free Expression Systems for Expression of Plasmodium Rhoptry Proteins. J Vis Exp. 2015(100):e52772. https://doi.org/10.3791/52772
Chen JH, Jung JW, Wang Y, Ha KS, Lu F, Lim CS, et al. Immunoproteomics profiling of blood stage Plasmodium vivax infection by high-throughput screening assays. J Proteome Res. 2010;9(12):6479-89. https://doi.org/10.1021/pr100705g
Lu F, Li J, Wang B, Cheng Y, Kong DH, Cui L, et al. Profiling the humoral immune responses to Plasmodium vivax infection and identification of candidate immunogenic rhoptry-associated membrane antigen (RAMA). J Proteomics. 2014;102:66-82. https://doi.org/10.1016/j.jprot.2014.02.029
Arevalo-Pinzon G, Gonzalez-Gonzalez M, Suarez CF, Curtidor H, Carabias-Sanchez J, Muro A, et al. Self-assembling functional programmable protein array for studying protein-protein interactions in malaria parasites. Malaria journal. 2018;17(1):270. https://doi.org/10.1186/s12936-018-2414-2
Takeo S, Arumugam TU, Torii M, Tsuboi T. Wheat germ cell-free technology for accelerating the malaria vaccine research. Expert Opin Drug Discov. 2009;4(11):1191-9. https://doi.org/10.1517/17460440903369813
Curtidor H, Patino LC, Arevalo-Pinzon G, Patarroyo ME, Patarroyo MA. Identification of the Plasmodium falciparum rhoptry neck protein 5 (PfRON5). Gene. 2011;474(1-2):22-8. https://doi.org/10.1016/j.gene.2010.12.005
Hossain ME, Dhawan S, Mohmmed A. The cysteine-rich regions of Plasmodium falciparum RON2 bind with host erythrocyte and AMA1 during merozoite invasion. Parasitol Res. 2012;110(5):1711-21. https://doi.org/10.1007/s00436-011-2690-z
Quintana MDP, Ch'ng JH, Zandian A, Imam M, Hultenby K, Theisen M, et al. SURGE complex of Plasmodium falciparum in the rhoptry-neck (SURFIN4.2-RON4-GLURP) contributes to merozoite invasion. PLoS One. 2018;13(8):e0201669. https://doi.org/10.1371/journal.pone.0201669
Gardiner DL, Spielmann T, Dixon MW, Hawthorne PL, Ortega MR, Anderson KL, et al. CLAG 9 is located in the rhoptries of Plasmodium falciparum. Parasitol Res. 2004;93(1):64-7. https://doi.org/10.1007/s00436-004-1098-4
Ito D, Takashima E, Yamasaki T, Hatano S, Hasegawa T, Miura K, et al. Antibodies against a Plasmodium falciparum RON12 inhibit merozoite invasion into erythrocytes. Parasitology international. 2019;68(1):87-91. https://doi.org/10.1016/j.parint.2018.10.006
Cheng Y, Wang B, Lu F, Ahmed MA, Han JH, Na SH, et al. Identification and characterization of Pv50, a novel Plasmodium vivax merozoite surface protein. Parasites & vectors. 2019;12(1):176. https://doi.org/10.1186/s13071-019-3434-7
Cheng Y, Li J, Ito D, Kong DH, Ha KS, Lu F, et al. Antigenicity and immunogenicity of PvRALP1, a novel Plasmodium vivax rhoptry neck protein. Malaria journal. 2015;14:186. https://doi.org/10.1186/s12936-015-0698-z
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