{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T04:22:10Z","timestamp":1772166130578,"version":"3.50.1"},"reference-count":65,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,5,16]],"date-time":"2024-05-16T00:00:00Z","timestamp":1715817600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,5,16]],"date-time":"2024-05-16T00:00:00Z","timestamp":1715817600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 201477\/Z\/16\/Z"],"award-info":[{"award-number":["Grant 201477\/Z\/16\/Z"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 206194"],"award-info":[{"award-number":["Grant 206194"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 206194"],"award-info":[{"award-number":["Grant 206194"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 206194"],"award-info":[{"award-number":["Grant 206194"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 206194"],"award-info":[{"award-number":["Grant 206194"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 206194"],"award-info":[{"award-number":["Grant 206194"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["Grant 201477\/Z\/16\/Z"],"award-info":[{"award-number":["Grant 201477\/Z\/16\/Z"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"The European Union\u2019s Horizon 2020 research and innovation programme","award":["Under grant agreement No 733273, \u2018Optimalvax\u2019"],"award-info":[{"award-number":["Under grant agreement No 733273, \u2018Optimalvax\u2019"]}]},{"name":"Cancer Research UK, the UK Medical Research Council, the Wellcome Trust","award":["Core Funding from The Francis Crick Institute"],"award-info":[{"award-number":["Core Funding from The Francis Crick Institute"]}]},{"name":"Cancer Research UK, the UK Medical Research Council, the Wellcome Trust","award":["Core Funding from The Francis Crick Institute"],"award-info":[{"award-number":["Core Funding from The Francis Crick Institute"]}]},{"name":"The Dutch Research Council (NOW) talent program veni","award":["VI.Veni.192.171"],"award-info":[{"award-number":["VI.Veni.192.171"]}]},{"name":"Medical Research Council","award":["Doctoral Training award MR\/J004111\/1"],"award-info":[{"award-number":["Doctoral Training award MR\/J004111\/1"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Malar J"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      Sporozoite invasion of hepatocytes is an essential step in the\n                      <jats:italic>Plasmodium<\/jats:italic>\n                      life-cycle and has similarities, at the cellular level, to merozoite invasion of erythrocytes. In the case of the\n                      <jats:italic>Plasmodium<\/jats:italic>\n                      blood-stage, efforts to identify host\u2013pathogen protein\u2013protein interactions have yielded important insights including vaccine candidates. In the case of sporozoite-hepatocyte invasion, the host\u2013pathogen protein\u2013protein interactions involved are poorly understood.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      To gain a better understanding of the protein\u2013protein interaction between the sporozoite ligands and host receptors, a systematic screen was performed. The previous\n                      <jats:italic>Plasmodium falciparum<\/jats:italic>\n                      and human surface protein ectodomain libraries were substantially extended, resulting in the creation of new libraries comprising 88\n                      <jats:italic>P. falciparum<\/jats:italic>\n                      sporozoite protein coding sequences and 182 sequences encoding human hepatocyte surface proteins. Having expressed recombinant proteins from these sequences, a plate-based assay was used, capable of detecting low affinity interactions between recombinant proteins, modified for enhanced throughput, to screen the proteins for interactions. The novel interactions identified in the screen were characterized biochemically, and their essential role in parasite invasion was further elucidated using antibodies and genetically manipulated\n                      <jats:italic>Plasmodium<\/jats:italic>\n                      parasites.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      A total of 7540 sporozoite-hepatocyte protein pairs were tested under conditions capable of detecting interactions of at least 1.2\u00a0\u00b5M\n                      <jats:italic>K<\/jats:italic>\n                      <jats:sub>D<\/jats:sub>\n                      . An interaction between the human fibroblast growth factor receptor 4 (FGFR4) and the\n                      <jats:italic>P. falciparum<\/jats:italic>\n                      protein Pf34 is identified and reported here, characterizing its affinity and demonstrating the blockade of the interaction by reagents, including a monoclonal antibody. Furthermore, further interactions between Pf34 and a second\n                      <jats:italic>P. falciparum<\/jats:italic>\n                      rhoptry neck protein, PfRON6, and between human low-density lipoprotein receptor (LDLR) and the\n                      <jats:italic>P. falciparum<\/jats:italic>\n                      protein PIESP15 are identified.\n                    <\/jats:p>\n                    <jats:p>Conditional genetic deletion confirmed the essentiality of PfRON6 in the blood-stage, consistent with the important role of this protein in parasite lifecycle. Pf34 was refractory to attempted genetic modification. Antibodies to Pf34 abrogated the interaction and had a modest effect upon sporozoite invasion into primary human hepatocytes.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>\n                      Pf34 and PfRON6 may be members of a functionally important invasion complex which could be a target for future interventions. The modified interaction screening assay, protein expression libraries and\n                      <jats:italic>P. falciparum<\/jats:italic>\n                      mutant parasites reported here may be a useful tool for protein interaction discovery and antigen candidate screening which could be of wider value to the scientific community.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12936-024-04913-2","type":"journal-article","created":{"date-parts":[[2024,5,16]],"date-time":"2024-05-16T13:01:58Z","timestamp":1715864518000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["A screen for Plasmodium falciparum sporozoite surface protein binding to human hepatocyte surface receptors identifies novel host\u2013pathogen interactions"],"prefix":"10.1186","volume":"23","author":[{"given":"Rameswara R.","family":"Segireddy","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hugo","family":"Belda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annie S. P.","family":"Yang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kirsten","family":"Dundas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julia","family":"Knoeckel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Francis","family":"Galaway","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laura","family":"Wood","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Doris","family":"Quinkert","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ellen","family":"Knuepfer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Moritz","family":"Treeck","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gavin J.","family":"Wright","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexander D.","family":"Douglas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,5,16]]},"reference":[{"key":"4913_CR1","volume-title":"World Malaria Report 2021","author":"WHO","year":"2021","unstructured":"WHO. World Malaria Report 2021. Geneva: World Health Organization; 2021."},{"key":"4913_CR2","doi-asserted-by":"publisher","first-page":"e1007943","DOI":"10.1371\/journal.ppat.1007943","volume":"15","author":"H Kumar","year":"2019","unstructured":"Kumar H, Tolia NH. Getting in: the structural biology of malaria invasion. PLoS Pathog. 2019;15:e1007943.","journal-title":"PLoS Pathog"},{"key":"4913_CR3","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1016\/j.pt.2008.08.006","volume":"24","author":"J Baum","year":"2008","unstructured":"Baum J, Gilberger TW, Frischknecht F, Meissner M. Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends Parasitol. 2008;24:557\u201363.","journal-title":"Trends Parasitol"},{"key":"4913_CR4","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1016\/j.chom.2017.07.003","volume":"22","author":"AF Cowman","year":"2017","unstructured":"Cowman AF, Tonkin CJ, Tham WH, Duraisingh MT. The molecular basis of erythrocyte invasion by malaria parasites. Cell Host Microbe. 2017;22:232\u201345.","journal-title":"Cell Host Microbe"},{"key":"4913_CR5","doi-asserted-by":"publisher","first-page":"4477","DOI":"10.1073\/pnas.1719660115","volume":"115","author":"K Dundas","year":"2018","unstructured":"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 Proc Natl Acad Sci USA. 2018;115:4477\u201382.","journal-title":"TRAP Proc Natl Acad Sci USA"},{"key":"4913_CR6","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.pt.2018.11.008","volume":"35","author":"K Dundas","year":"2019","unstructured":"Dundas K, Shears MJ, Sinnis P, Wright GJ. Important extracellular interactions between Plasmodium sporozoites and host cells required for infection. Trends Parasitol. 2019;35:129\u201339.","journal-title":"Trends Parasitol"},{"key":"4913_CR7","doi-asserted-by":"publisher","first-page":"e1000010","DOI":"10.1371\/journal.ppat.1000010","volume":"4","author":"S Yalaoui","year":"2008","unstructured":"Yalaoui S, Zougbede S, Charrin S, Silvie O, Arduise C, Farhati K, et al. Hepatocyte permissiveness to Plasmodium infection is conveyed by a short and structurally conserved region of the CD81 large extracellular domain. PLoS Pathog. 2008;4:e1000010.","journal-title":"PLoS Pathog"},{"key":"4913_CR8","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/j.chom.2008.07.012","volume":"4","author":"CD Rodrigues","year":"2008","unstructured":"Rodrigues CD, Hannus M, Prudencio M, Martin C, Goncalves LA, Portugal S, et al. Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe. 2008;4:271\u201382.","journal-title":"Cell Host Microbe"},{"key":"4913_CR9","doi-asserted-by":"publisher","first-page":"1134","DOI":"10.1111\/j.1462-5822.2006.00697.x","volume":"8","author":"O Silvie","year":"2006","unstructured":"Silvie O, Greco C, Franetich JF, Dubart-Kupperschmitt A, Hannoun L, van Gemert GJ, et al. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell Microbiol. 2006;8:1134\u201346.","journal-title":"Cell Microbiol"},{"key":"4913_CR10","doi-asserted-by":"publisher","first-page":"e25903","DOI":"10.7554\/eLife.25903","volume":"6","author":"G Manzoni","year":"2017","unstructured":"Manzoni G, Marinach C, Topcu S, Briquet S, Grand M, Tolle M, et al. Plasmodium P36 determines host cell receptor usage during sporozoite invasion. Elife. 2017;6:e25903.","journal-title":"Elife"},{"key":"4913_CR11","doi-asserted-by":"publisher","first-page":"1287","DOI":"10.1084\/jem.177.5.1287","volume":"177","author":"U Frevert","year":"1993","unstructured":"Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med. 1993;177:1287\u201398.","journal-title":"J Exp Med"},{"key":"4913_CR12","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1016\/j.chom.2007.10.002","volume":"2","author":"A Coppi","year":"2007","unstructured":"Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, et al. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2007;2:316\u201327.","journal-title":"Cell Host Microbe"},{"key":"4913_CR13","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1126\/science.aad3318","volume":"350","author":"A Kaushansky","year":"2015","unstructured":"Kaushansky A, Douglass AN, Arang N, Vigdorovich V, Dambrauskas N, Kain HS, et al. Malaria parasites target the hepatocyte receptor EphA2 for successful host infection. Science. 2015;350:1089\u201392.","journal-title":"Science"},{"key":"4913_CR14","doi-asserted-by":"publisher","first-page":"e0200032","DOI":"10.1371\/journal.pone.0200032","volume":"13","author":"AC Langlois","year":"2018","unstructured":"Langlois AC, Marinach C, Manzoni G, Silvie O. Plasmodium sporozoites can invade hepatocytic cells independently of the Ephrin receptor A2. PLoS ONE. 2018;13:e0200032.","journal-title":"PLoS ONE"},{"key":"4913_CR15","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1038\/nature10606","volume":"480","author":"C Crosnier","year":"2011","unstructured":"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;480:534\u20137.","journal-title":"Nature"},{"key":"4913_CR16","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1101\/gr.7187808","volume":"18","author":"KM Bushell","year":"2008","unstructured":"Bushell KM, Sollner C, Schuster-Boeckler B, Bateman A, Wright GJ. Large-scale screening for novel low-affinity extracellular protein interactions. Genome Res. 2008;18:622\u201330.","journal-title":"Genome Res"},{"key":"4913_CR17","doi-asserted-by":"publisher","first-page":"100038","DOI":"10.1074\/mcp.RA120.002432","volume":"20","author":"J Knockel","year":"2021","unstructured":"Knockel J, Dundas K, Yang ASP, Galaway F, Metcalf T, Gemert GV, et al. Systematic identification of Plasmodium falciparum sporozoite membrane protein interactions reveals an essential role for the p24 complex in host infection. Mol Cell Proteomics. 2021;20:100038.","journal-title":"Mol Cell Proteomics"},{"key":"4913_CR18","doi-asserted-by":"publisher","first-page":"e1005606","DOI":"10.1371\/journal.ppat.1005606","volume":"12","author":"KE Swearingen","year":"2016","unstructured":"Swearingen KE, Lindner SE, Shi L, Shears MJ, Harupa A, Hopp CS, et al. Interrogating the Plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics. PLoS Pathog. 2016;12:e1005606.","journal-title":"PLoS Pathog"},{"key":"4913_CR19","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.1074\/mcp.M112.024505","volume":"12","author":"SE Lindner","year":"2013","unstructured":"Lindner SE, Swearingen KE, Harupa A, Vaughan AM, Sinnis P, Moritz RL, et al. Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol Cell Proteomics. 2013;12:1127\u201343.","journal-title":"Mol Cell Proteomics"},{"key":"4913_CR20","doi-asserted-by":"publisher","first-page":"e1000195","DOI":"10.1371\/journal.ppat.1000195","volume":"4","author":"E Lasonder","year":"2008","unstructured":"Lasonder E, Janse CJ, van Gemert GJ, Mair GR, Vermunt AM, Douradinha BG, et al. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog. 2008;4:e1000195.","journal-title":"PLoS Pathog"},{"key":"4913_CR21","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.1126\/science.1087025","volume":"301","author":"KG Le Roch","year":"2003","unstructured":"Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science. 2003;301:1503\u20138.","journal-title":"Science"},{"key":"4913_CR22","doi-asserted-by":"publisher","first-page":"1142","DOI":"10.1002\/pmic.200800404","volume":"9","author":"K Lal","year":"2009","unstructured":"Lal K, Prieto JH, Bromley E, Sanderson SJ, Yates JR 3rd, Wastling JM, et al. Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics. 2009;9:1142\u201351.","journal-title":"Proteomics"},{"key":"4913_CR23","doi-asserted-by":"publisher","first-page":"995","DOI":"10.1021\/pr049926m","volume":"3","author":"TY Sam-Yellowe","year":"2004","unstructured":"Sam-Yellowe TY, Florens L, Wang T, Raine JD, Carucci DJ, Sinden R, et al. Proteome analysis of rhoptry-enriched fractions isolated from Plasmodium merozoites. J Proteome Res. 2004;3:995\u20131001.","journal-title":"J Proteome Res"},{"key":"4913_CR24","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1007\/978-1-62703-026-7_9","volume":"923","author":"SM Khan","year":"2013","unstructured":"Khan SM, Kroeze H, Franke-Fayard B, Janse CJ. Standardization in generating and reporting genetically modified rodent malaria parasites: the RMgmDB database. Methods Mol Biol. 2013;923:139\u201350.","journal-title":"Methods Mol Biol"},{"key":"4913_CR25","doi-asserted-by":"publisher","first-page":"e24109","DOI":"10.7554\/eLife.24109","volume":"6","author":"JM Santos","year":"2017","unstructured":"Santos JM, Egarter S, Zuzarte-Luis V, Kumar H, Moreau CA, Kehrer J, et al. Malaria parasite LIMP protein regulates sporozoite gliding motility and infectivity in mosquito and mammalian hosts. Elife. 2017;6:e24109.","journal-title":"Elife"},{"key":"4913_CR26","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1186\/1475-2875-8-235","volume":"8","author":"TV Nguyen","year":"2009","unstructured":"Nguyen TV, Sacci JB Jr, de la Vega P, John CC, James AA, Kang AS. Characterization of immunoglobulin G antibodies to Plasmodium falciparum sporozoite surface antigen MB2 in malaria exposed individuals. Malar J. 2009;8:235.","journal-title":"Malar J"},{"key":"4913_CR27","doi-asserted-by":"publisher","first-page":"3845","DOI":"10.1128\/IAI.69.6.3845-3952.2001","volume":"69","author":"K Brahimi","year":"2001","unstructured":"Brahimi K, Badell E, Sauzet JP, BenMohamed L, Daubersies P, Guerin-Marchand C, et al. Human antibodies against Plasmodium falciparum liver-stage antigen 3 cross-react with Plasmodium yoelii preerythrocytic-stage epitopes and inhibit sporozoite invasion in vitro and in vivo. Infect Immun. 2001;69:3845\u201352.","journal-title":"Infect Immun"},{"key":"4913_CR28","doi-asserted-by":"publisher","first-page":"2502","DOI":"10.1002\/eji.1830271007","volume":"27","author":"DA Fidock","year":"1997","unstructured":"Fidock DA, Pasquetto V, Gras H, Badell E, Eling W, Ballou WR, et al. Plasmodium falciparum sporozoite invasion is inhibited by naturally acquired or experimentally induced polyclonal antibodies to the STARP antigen. Eur J Immunol. 1997;27:2502\u201313.","journal-title":"Eur J Immunol"},{"key":"4913_CR29","doi-asserted-by":"publisher","first-page":"3976","DOI":"10.1074\/mcp.O113.028357","volume":"12","author":"C Crosnier","year":"2013","unstructured":"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 Proteom. 2013;12:3976\u201386.","journal-title":"Mol Cell Proteom"},{"key":"4913_CR30","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1016\/j.jprot.2016.01.016","volume":"136","author":"JR Wisniewski","year":"2016","unstructured":"Wisniewski JR, Vildhede A, Noren A, Artursson P. In-depth quantitative analysis and comparison of the human hepatocyte and hepatoma cell line HepG2 proteomes. J Proteom. 2016;136:234\u201347.","journal-title":"J Proteom"},{"key":"4913_CR31","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1002\/prca.201400194","volume":"9","author":"A Ducret","year":"2015","unstructured":"Ducret A, Kux van Geijtenbeek S, Roder D, Simon S, Chin D, Berrera M, et al. Identification of six cell surface proteins for specific liver targeting. Proteom Clin Appl. 2015;9:651\u201361.","journal-title":"Proteom Clin Appl"},{"key":"4913_CR32","doi-asserted-by":"publisher","first-page":"1153","DOI":"10.1074\/mcp.M113.035584","volume":"13","author":"D Tao","year":"2014","unstructured":"Tao D, King JG, Tweedell RE, Jost PJ, Boddey JA, Dinglasan RR. The acute transcriptomic and proteomic response of HC-04 hepatoma cells to hepatocyte growth factor and its implications for Plasmodium falciparum sporozoite invasion. Mol Cell Proteom. 2014;13:1153\u201364.","journal-title":"Mol Cell Proteom"},{"key":"4913_CR33","doi-asserted-by":"publisher","first-page":"1260419","DOI":"10.1126\/science.1260419","volume":"347","author":"M Uhlen","year":"2015","unstructured":"Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347:1260419.","journal-title":"Science"},{"key":"4913_CR34","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1038\/s41586-022-05028-x","volume":"608","author":"J Shilts","year":"2022","unstructured":"Shilts J, Severin Y, Galaway F, Muller-Sienerth N, Chong ZS, Pritchard S, et al. A physical wiring diagram for the human immune system. Nature. 2022;608:397\u2013404.","journal-title":"Nature"},{"key":"4913_CR35","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1074\/mcp.M114.046946","volume":"14","author":"Y Sun","year":"2015","unstructured":"Sun Y, Vandenbriele C, Kauskot A, Verhamme P, Hoylaerts MF, Wright GJ. A human platelet receptor protein microarray identifies the high affinity immunoglobulin E receptor subunit alpha (FcepsilonR1alpha) as an activating platelet endothelium aggregation receptor 1 (PEAR1) ligand. Mol Cell Proteom. 2015;14:1265\u201374.","journal-title":"Mol Cell Proteom"},{"key":"4913_CR36","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1038\/nm808","volume":"9","author":"O Silvie","year":"2003","unstructured":"Silvie O, Rubinstein E, Franetich JF, Prenant M, Belnoue E, Renia L, et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med. 2003;9:93\u20136.","journal-title":"Nat Med"},{"key":"4913_CR37","doi-asserted-by":"publisher","first-page":"938","DOI":"10.1126\/science.282.5390.938","volume":"282","author":"P Pileri","year":"1998","unstructured":"Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, et al. Binding of hepatitis C virus to CD81. Science. 1998;282:938\u201341.","journal-title":"Science"},{"key":"4913_CR38","doi-asserted-by":"publisher","first-page":"E9","DOI":"10.1093\/nar\/30.2.e9","volume":"30","author":"Y Durocher","year":"2002","unstructured":"Durocher Y, Perret S, Kamen A. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 2002;30:E9.","journal-title":"Nucleic Acids Res"},{"key":"4913_CR39","doi-asserted-by":"publisher","first-page":"1233","DOI":"10.1016\/j.ijpara.2007.03.013","volume":"37","author":"NI Proellocks","year":"2007","unstructured":"Proellocks NI, Kovacevic S, Ferguson DJ, Kats LM, Morahan BJ, Black CG, et al. Plasmodium falciparum Pf34, a novel GPI-anchored rhoptry protein found in detergent-resistant microdomains. Int J Parasitol. 2007;37:1233\u201341.","journal-title":"Int J Parasitol"},{"key":"4913_CR40","doi-asserted-by":"publisher","first-page":"15292","DOI":"10.1074\/jbc.271.25.15292","volume":"271","author":"DM Ornitz","year":"1996","unstructured":"Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, et al. Receptor specificity of the fibroblast growth factor family. J Biol Chem. 1996;271:15292\u20137.","journal-title":"J Biol Chem"},{"key":"4913_CR41","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1016\/j.jmb.2010.07.001","volume":"402","author":"EJ De Genst","year":"2010","unstructured":"De Genst EJ, Guilliams T, Wellens J, O\u2019Day EM, Waudby CA, Meehan S, et al. Structure and properties of a complex of alpha-synuclein and a single-domain camelid antibody. J Mol Biol. 2010;402:326\u201343.","journal-title":"J Mol Biol"},{"key":"4913_CR42","unstructured":"GENENTECH IUUDW, South San Francisco, California 94080 (US). Anti-fgfr4 antibodies and methods of use. In: International Application Published Under The Patent Cooperation Treaty (PCT) (Bureau WIPOI ed. USA, 2012."},{"key":"4913_CR43","doi-asserted-by":"publisher","first-page":"e106583","DOI":"10.15252\/embj.2020106583","volume":"40","author":"ASP Yang","year":"2021","unstructured":"Yang ASP, van Waardenburg YM, van de Vegte-Bolmer M, van Gemert GA, Graumans W, de Wilt JHW, et al. Zonal human hepatocytes are differentially permissive to Plasmodium falciparum malaria parasites. EMBO J. 2021;40:e106583.","journal-title":"EMBO J"},{"key":"4913_CR44","doi-asserted-by":"publisher","first-page":"e1002991","DOI":"10.1371\/journal.ppat.1002991","volume":"8","author":"AR Williams","year":"2012","unstructured":"Williams AR, Douglas AD, Miura K, Illingworth JJ, Choudhary P, Murungi LM, et al. Enhancing blockade of Plasmodium falciparum erythrocyte invasion: assessing combinations of antibodies against PfRH5 and other merozoite antigens. PLoS Pathog. 2012;8:e1002991.","journal-title":"PLoS Pathog"},{"key":"4913_CR45","doi-asserted-by":"publisher","first-page":"e01170","DOI":"10.1128\/mBio.01170-19","volume":"10","author":"M Tiburcio","year":"2019","unstructured":"Tiburcio M, Yang ASP, Yahata K, Suarez-Cortes P, Belda H, Baumgarten S, et al. A novel tool for the generation of conditional knockouts to study gene function across the Plasmodium falciparum life cycle. mBio. 2019;10:e01170-19.","journal-title":"mBio"},{"key":"4913_CR46","doi-asserted-by":"publisher","first-page":"3881","DOI":"10.1038\/s41598-017-03984-3","volume":"7","author":"E Knuepfer","year":"2017","unstructured":"Knuepfer E, Napiorkowska M, van Ooij C, Holder AA. Generating conditional gene knockouts in Plasmodium - a toolkit to produce stable DiCre recombinase-expressing parasite lines using CRISPR\/Cas9. Sci Rep. 2017;7:3881.","journal-title":"Sci Rep"},{"key":"4913_CR47","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1038\/s41564-020-0702-4","volume":"5","author":"H Davies","year":"2020","unstructured":"Davies H, Belda H, Broncel M, Ye X, Bisson C, Introini V, et al. An exported kinase family mediates species-specific erythrocyte remodelling and virulence in human malaria. Nat Microbiol. 2020;5:848\u201363.","journal-title":"Nat Microbiol"},{"key":"4913_CR48","doi-asserted-by":"publisher","first-page":"10522","DOI":"10.1038\/s41598-020-67468-7","volume":"10","author":"F Galaway","year":"2020","unstructured":"Galaway F, Wright GJ. Rapid and sensitive large-scale screening of low affinity extracellular receptor protein interactions by using reaction induced inhibition of Gaussia luciferase. Sci Rep. 2020;10:10522.","journal-title":"Sci Rep"},{"key":"4913_CR49","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1038\/nature13203","volume":"508","author":"E Bianchi","year":"2014","unstructured":"Bianchi E, Doe B, Goulding D, Wright GJ. Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature. 2014;508:483\u20137.","journal-title":"Nature"},{"key":"4913_CR50","doi-asserted-by":"publisher","first-page":"1466","DOI":"10.1111\/j.1462-5822.2006.00885.x","volume":"9","author":"J Thompson","year":"2007","unstructured":"Thompson J, Fernandez-Reyes D, Sharling L, Moore SG, Eling WM, Kyes SA, et al. Plasmodium cysteine repeat modular proteins 1\u20134: complex proteins with roles throughout the malaria parasite life cycle. Cell Microbiol. 2007;9:1466\u201380.","journal-title":"Cell Microbiol"},{"key":"4913_CR51","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1016\/j.cell.2017.06.030","volume":"170","author":"E Bushell","year":"2017","unstructured":"Bushell E, Gomes AR, Sanderson T, Anar B, Girling G, Herd C, et al. Functional profiling of a Plasmodium genome reveals an abundance of essential genes. Cell. 2017;170:260-72.e8.","journal-title":"Cell"},{"key":"4913_CR52","doi-asserted-by":"publisher","first-page":"1112","DOI":"10.1016\/j.cell.2019.10.030","volume":"179","author":"RR Stanway","year":"2019","unstructured":"Stanway RR, Bushell E, Chiappino-Pepe A, Roques M, Sanderson T, Franke-Fayard B, et al. Genome-scale identification of essential metabolic processes for targeting the Plasmodium liver stage. Cell. 2019;179:1112-28.e26.","journal-title":"Cell"},{"key":"4913_CR53","doi-asserted-by":"publisher","first-page":"2881","DOI":"10.2174\/13816128113199990594","volume":"20","author":"C Heinzle","year":"2014","unstructured":"Heinzle C, Erdem Z, Paur J, Grasl-Kraupp B, Holzmann K, Grusch M, et al. Is fibroblast growth factor receptor 4 a suitable target of cancer therapy? Curr Pharm Des. 2014;20:2881\u201398.","journal-title":"Curr Pharm Des"},{"key":"4913_CR54","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1021\/mp700105z","volume":"5","author":"S Jones","year":"2008","unstructured":"Jones S. Mini-review: endocrine actions of fibroblast growth factor 19. Mol Pharm. 2008;5:42\u20138.","journal-title":"Mol Pharm"},{"key":"4913_CR55","doi-asserted-by":"publisher","first-page":"1232","DOI":"10.1038\/s41467-017-01345-2","volume":"8","author":"N Arang","year":"2017","unstructured":"Arang N, Kain HS, Glennon EK, Bello T, Dudgeon DR, Walter ENF, et al. Identifying host regulators and inhibitors of liver stage malaria infection using kinase activity profiles. Nat Commun. 2017;8:1232.","journal-title":"Nat Commun"},{"key":"4913_CR56","doi-asserted-by":"publisher","first-page":"e1000201","DOI":"10.1371\/journal.ppat.1000201","volume":"4","author":"M Prudencio","year":"2008","unstructured":"Prudencio M, Rodrigues CD, Hannus M, Martin C, Real E, Goncalves LA, et al. Kinome-wide RNAi screen implicates at least 5 host hepatocyte kinases in Plasmodium sporozoite infection. PLoS Pathog. 2008;4:e1000201.","journal-title":"PLoS Pathog"},{"key":"4913_CR57","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1126\/science.2544996","volume":"245","author":"PL Lee","year":"1989","unstructured":"Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT. Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science. 1989;245:57\u201360.","journal-title":"Science"},{"key":"4913_CR58","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1002\/wdev.176","volume":"4","author":"DM Ornitz","year":"2015","unstructured":"Ornitz DM, Itoh N. The Fibroblast Growth Factor signaling pathway. Wiley Interdiscip Rev Dev Biol. 2015;4:215\u201366.","journal-title":"Wiley Interdiscip Rev Dev Biol"},{"key":"4913_CR59","doi-asserted-by":"publisher","first-page":"1179","DOI":"10.1073\/pnas.1415466112","volume":"112","author":"KS Reddy","year":"2015","unstructured":"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. Proc Natl Acad Sci USA. 2015;112:1179\u201384.","journal-title":"Proc Natl Acad Sci USA"},{"key":"4913_CR60","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1016\/j.ijpara.2008.11.002","volume":"39","author":"NI Proellocks","year":"2009","unstructured":"Proellocks NI, Kats LM, Sheffield DA, Hanssen E, Black CG, Waller KL, et al. Characterisation of PfRON6, a Plasmodium falciparum rhoptry neck protein with a novel cysteine-rich domain. Int J Parasitol. 2009;39:683\u201392.","journal-title":"Int J Parasitol"},{"key":"4913_CR61","doi-asserted-by":"publisher","first-page":"e1010643","DOI":"10.1371\/journal.ppat.1010643","volume":"18","author":"P Fernandes","year":"2022","unstructured":"Fernandes P, Loubens M, Le Borgne R, Marinach C, Ardin B, Briquet S, et al. The AMA1-RON complex drives Plasmodium sporozoite invasion in the mosquito and mammalian hosts. PLoS Pathog. 2022;18:e1010643.","journal-title":"PLoS Pathog"},{"key":"4913_CR62","doi-asserted-by":"publisher","first-page":"e36713","DOI":"10.1371\/journal.pone.0036713","volume":"7","author":"DM French","year":"2012","unstructured":"French DM, Lin BC, Wang M, Adams C, Shek T, Hotzel K, et al. Targeting FGFR4 inhibits hepatocellular carcinoma in preclinical mouse models. PLoS ONE. 2012;7:e36713.","journal-title":"PLoS ONE"},{"key":"4913_CR63","doi-asserted-by":"publisher","first-page":"7847","DOI":"10.1126\/science.aap7847","volume":"360","author":"M Zhang","year":"2018","unstructured":"Zhang M, Wang C, Otto TD, Oberstaller J, Liao X, Adapa SR, et al. Uncovering the essential genes of the human malaria parasite Plasmodium falciparum by saturation mutagenesis. Science. 2018;360:7847.","journal-title":"Science"},{"key":"4913_CR64","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1038\/nature25010","volume":"553","author":"S Lee","year":"2018","unstructured":"Lee S, Choi J, Mohanty J, Sousa LP, Tome F, Pardon E, et al. Structures of beta-klotho reveal a \u2019zip code\u2019-like mechanism for endocrine FGF signalling. Nature. 2018;553:501\u20135.","journal-title":"Nature"},{"key":"4913_CR65","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1016\/S1074-7613(00)00023-6","volume":"13","author":"GJ Wright","year":"2000","unstructured":"Wright GJ, Puklavec MJ, Willis AC, Hoek RM, Sedgwick JD, Brown MH, et al. Lymphoid\/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity. 2000;13:233\u201342.","journal-title":"Immunity"}],"container-title":["Malaria Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12936-024-04913-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12936-024-04913-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12936-024-04913-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,16]],"date-time":"2024-05-16T13:02:22Z","timestamp":1715864542000},"score":1,"resource":{"primary":{"URL":"https:\/\/malariajournal.biomedcentral.com\/articles\/10.1186\/s12936-024-04913-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,16]]},"references-count":65,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["4913"],"URL":"https:\/\/doi.org\/10.1186\/s12936-024-04913-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.02.02.929190","asserted-by":"object"}]},"ISSN":["1475-2875"],"issn-type":[{"value":"1475-2875","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,16]]},"assertion":[{"value":"7 December 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 March 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 May 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Ethics statement is described in the Methods section.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"151"}}