{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,18]],"date-time":"2026-07-18T06:26:43Z","timestamp":1784356003272,"version":"3.55.0"},"reference-count":72,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,1,8]],"date-time":"2021-01-08T00:00:00Z","timestamp":1610064000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100015691","name":"Division of Microbiology and Infectious Diseases, National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["U19AI089681, AI45999"],"award-info":[{"award-number":["U19AI089681, AI45999"]}],"id":[{"id":"10.13039\/100015691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["P41GM103533"],"award-info":[{"award-number":["P41GM103533"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>Malaria parasites are transmitted by\u00a0<jats:italic>Anopheles<\/jats:italic>\u00a0mosquitoes. During its life cycle in the mosquito vector the <jats:italic>Plasmodium<\/jats:italic> ookinete escapes the proteolytic milieu of the post-blood meal midgut by traversing the midgut wall. This process requires penetration of the chitin-containing peritrophic matrix lining the midgut epithelium, which depends in part on ookinete-secreted chitinases. <jats:italic>Plasmodium falciparum<\/jats:italic> ookinetes have one chitinase (PfCHT1), whereas ookinetes of the avian-infecting parasite, <jats:italic>P. gallinaceum<\/jats:italic>, have two, a long and a short form, PgCHT1 and PgCHT2, respectively. Published data indicates that PgCHT2 forms a high molecular weight (HMW) reduction-sensitive complex; and one binding partner is the ookinete-produced von Willebrand A-domain-containing protein, WARP. Size exclusion chromatography data reported here show that <jats:italic>P. gallinaceum<\/jats:italic> PgCHT2 and its ortholog, <jats:italic>P. falciparum<\/jats:italic> PfCHT1 are covalently-linked components of a HMW chitinase-containing complex (&amp;gt; 1,300 kDa). Mass spectrometry of ookinete-secreted proteins isolated using a new chitin bead pull-down method identified chitinase-associated proteins in <jats:italic>P. falciparum<\/jats:italic> and <jats:italic>P. gallinaceum<\/jats:italic> ookinete-conditioned culture media. Mass spectrometry of this complex showed the presence of several micronemal proteins including von Willebrand factor A domain-related protein (WARP), ookinete surface enolase, and secreted ookinete adhesive protein (SOAP). To test the hypothesis that ookinete-produced PfCHT1 can form a high molecular homo-multimer or, alternatively, interacts with <jats:italic>P. berghei<\/jats:italic> ookinete-produced proteins to produce an HMW hetero-multimer, we created chimeric <jats:italic>P. berghei<\/jats:italic> parasites expressing <jats:italic>PfCHT1<\/jats:italic> to replace <jats:italic>PbCHT<\/jats:italic>1, enabling the production of large numbers of PfCHT1-expressing ookinetes. We show that chimeric <jats:italic>P. berghei<\/jats:italic> ookinetes express monomeric PfCHT1, but a HMW complex containing <jats:italic>PfCHT1<\/jats:italic> is not present. A better understanding of the chitinase-containing HMW complex may enhance development of next-generation vaccines or drugs that target malaria transmission stages.<\/jats:p>","DOI":"10.3389\/fcimb.2020.615343","type":"journal-article","created":{"date-parts":[[2021,1,9]],"date-time":"2021-01-09T01:57:32Z","timestamp":1610157452000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["A Hetero-Multimeric Chitinase-Containing Plasmodium falciparum and Plasmodium gallinaceum Ookinete-Secreted Protein Complex Involved in Mosquito Midgut Invasion"],"prefix":"10.3389","volume":"10","author":[{"given":"Kailash P.","family":"Patra","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hargobinder","family":"Kaur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Surendra Kumar","family":"Kolli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacob M.","family":"Wozniak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Judith Helena","family":"Prieto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"III","given":"John R.","family":"Yates","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David J.","family":"Gonzalez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chris J.","family":"Janse","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph M.","family":"Vinetz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,1,8]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"5573","DOI":"10.1074\/jbc.M307582200","article-title":"Analysis of the Plasmodium and Anopheles transcriptional repertoire during ookinete development and midgut invasion","volume":"279","author":"Abraham","year":"2004","journal-title":"J. Biol. Chem."},{"key":"B2","doi-asserted-by":"publisher","first-page":"532","DOI":"10.1038\/nsmb.3048","article-title":"The Anopheles-midgut APN1 structure reveals a new malaria transmission-blocking vaccine epitope","volume":"22","author":"Atkinson","year":"2015","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/mBio.01656-17","article-title":"Plasmodium falciparum Calcium-Dependent Protein Kinase 2 Is Critical for Male Gametocyte Exflagellation but Not Essential for Asexual Proliferation","volume":"8","author":"Bansal","year":"2017","journal-title":"MBio"},{"key":"B4","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1111\/cmi.12604","article-title":"The development of malaria parasites in the mosquito midgut","volume":"18","author":"Bennink","year":"2016","journal-title":"Cell Microbiol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1187","DOI":"10.4269\/ajtmh.2010.10-0433","article-title":"In vitro generation of Plasmodium falciparum ookinetes","volume":"83","author":"Bounkeua","year":"2010","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"B6","doi-asserted-by":"publisher","first-page":"5863","DOI":"10.1016\/j.vaccine.2016.10.027","article-title":"Utilizing direct skin feeding assays for development of vaccines that interrupt malaria transmission: A systematic review of methods and case study","volume":"34","author":"Brickley","year":"2016","journal-title":"Vaccine"},{"key":"B7","doi-asserted-by":"publisher","first-page":"57","DOI":"10.4269\/ajtmh.15-0007","article-title":"Antimalarial Drug Resistance: Literature Review and Activities and Findings of the ICEMR Network","volume":"93","author":"Cui","year":"2015","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1518","DOI":"10.1016\/j.vaccine.2015.01.050","article-title":"Design of a Phase III cluster randomized trial to assess the efficacy and safety of a malaria transmission blocking vaccine","volume":"33","author":"Delrieu","year":"2015","journal-title":"Vaccine"},{"key":"B9","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1016\/j.pt.2018.07.001","article-title":"Antimalarial Transmission-Blocking Interventions: Past, Present, and Future","volume":"34","author":"Delves","year":"2018","journal-title":"Trends Parasitol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmicb.2019.02134","article-title":"Fueling Open Innovation for Malaria Transmission-Blocking Drugs: Hundreds of Molecules Targeting Early Parasite Mosquito Stages","volume":"10","author":"Delves","year":"2019","journal-title":"Front. Microbiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"4041","DOI":"10.1128\/IAI.69.6.4041-4047.2001","article-title":"Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes","volume":"69","author":"Dessens","year":"2001","journal-title":"Infect. Immun."},{"key":"B12","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1046\/j.1365-2958.2003.03566.x","article-title":"SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development","volume":"49","author":"Dessens","year":"2003","journal-title":"Mol. Microbiol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1016\/j.pt.2008.05.002","article-title":"Flipping the paradigm on malaria transmission-blocking vaccines","volume":"24","author":"Dinglasan","year":"2008","journal-title":"Trends Parasitol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"15882","DOI":"10.1073\/pnas.0706340104","article-title":"Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion","volume":"104","author":"Dinglasan","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B15","doi-asserted-by":"publisher","first-page":"13461","DOI":"10.1073\/pnas.0702239104","article-title":"Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen","volume":"104","author":"Dinglasan","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B16","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1038\/s41541-020-0196-3","article-title":"Malaria vaccines since 2000: progress, priorities, products","volume":"5","author":"Duffy","year":"2020","journal-title":"NPJ Vaccines"},{"key":"B17","doi-asserted-by":"publisher","first-page":"976","DOI":"10.1016\/1044-0305(94)80016-2","article-title":"An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database","volume":"5","author":"Eng","year":"1994","journal-title":"J.\u00a0Am. Soc. Mass Spectrom."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/IAI.00498-16","article-title":"The Plasmodium falciparum Cell-Traversal Protein for Ookinetes and Sporozoites as a Candidate for Preerythrocytic and Transmission-Blocking Vaccines","volume":"85","author":"Espinosa","year":"2017","journal-title":"Infect. Immun."},{"key":"B19","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1186\/1475-2875-9-194","article-title":"An improved method for the in vitro differentiation of Plasmodium falciparum gametocytes into ookinetes","volume":"9","author":"Ghosh","year":"2010","journal-title":"Malar. J."},{"key":"B20","doi-asserted-by":"publisher","first-page":"17153","DOI":"10.1073\/pnas.1103657108","article-title":"Plasmodium ookinetes coopt mammalian plasminogen to invade the mosquito midgut","volume":"108","author":"Ghosh","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B21","doi-asserted-by":"publisher","first-page":"3313","DOI":"10.1042\/BCJ20190633","article-title":"Phosphorylation of human placental aromatase CYP19A1","volume":"476","author":"Ghosh","year":"2019","journal-title":"Biochem. J."},{"key":"B22","doi-asserted-by":"publisher","first-page":"7315","DOI":"10.1016\/j.vaccine.2016.10.090","article-title":"Report from the World Health Organization\u2019s third Product Development for Vaccines Advisory Committee (PDVAC) meeting, Geneva, 8-10th June 2016","volume":"37","author":"Giersing","year":"2019","journal-title":"Vaccine"},{"key":"B23","doi-asserted-by":"publisher","first-page":"S23","DOI":"10.1016\/S0163-4453(17)30187-1","article-title":"New tools for malaria control - using them wisely","author":"Greenwood","year":"2017","journal-title":"J. Infect."},{"key":"B24","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1093\/bioinformatics\/9.2.161","article-title":"MASCOT: multiple alignment system for protein sequences based on three-way dynamic programming","volume":"9","author":"Hirosawa","year":"1993","journal-title":"Comput. Appl. Biosci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"2807","DOI":"10.1073\/pnas.88.7.2807","article-title":"Malaria parasite chitinase and penetration of the mosquito peritrophic membrane","volume":"88","author":"Huber","year":"1991","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B26","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1016\/0169-4758(95)80133-2","article-title":"Plasmodium berghei: the application of cultivation and purification techniques to molecular studies of malaria parasites","volume":"11","author":"Janse","year":"1995","journal-title":"Parasitol. Today"},{"key":"B27","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1017\/S0031182000056481","article-title":"In vitro formation of ookinetes and functional maturity of Plasmodium berghei gametocytes","volume":"91","author":"Janse","year":"1985","journal-title":"Parasitology"},{"key":"B28","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1038\/nprot.2006.53","article-title":"High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei","volume":"1","author":"Janse","year":"2006","journal-title":"Nat. Protoc."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-03984-3","article-title":"Generating conditional gene knockouts in Plasmodium - a toolkit to produce stable DiCre recombinase-expressing parasite lines using CRISPR\/Cas9","volume":"7","author":"Knuepfer","year":"2017","journal-title":"Sci. Rep."},{"key":"B30","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1016\/S1471-4922(01)01918-3","article-title":"Plasmodium ookinete-secreted chitinase and parasite penetration of the mosquito peritrophic matrix","volume":"17","author":"Langer","year":"2001","journal-title":"Trends Parasitol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"6461","DOI":"10.1128\/IAI.68.11.6461-6465.2000","article-title":"Micronemal transport of Plasmodium ookinete chitinases to the electron-dense area of the apical complex for extracellular secretion","volume":"68","author":"Langer","year":"2000","journal-title":"Infect. Immun."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1581","DOI":"10.1128\/IAI.70.3.1581-1590.2002","article-title":"Monoclonal antibody against the Plasmodium falciparum chitinase, PfCHT1, recognizes a malaria transmission-blocking epitope in Plasmodium gallinaceum ookinetes unrelated to the chitinase PgCHT1","volume":"70","author":"Langer","year":"2002","journal-title":"Infect. Immun."},{"key":"B33","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1128\/IAI.70.1.102-106.2002","article-title":"Identification of novel Plasmodium gallinaceum zygote- and ookinete-expressed proteins as targets for blocking malaria transmission","volume":"70","author":"Langer","year":"2002","journal-title":"Infect. Immun."},{"key":"B34","doi-asserted-by":"publisher","first-page":"26635","DOI":"10.1074\/jbc.M401385200","article-title":"Plasmodium ookinete-secreted proteins secreted through a common micronemal pathway are targets of blocking malaria transmission","volume":"279","author":"Li","year":"2004","journal-title":"J. Biol. Chem."},{"key":"B35","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1086\/432552","article-title":"An anti-Chitinase malaria transmission-blocking single-chain antibody as an effector molecule for creating a Plasmodium falciparum-refractory mosquito","volume":"192","author":"Li","year":"2005","journal-title":"J. Infect. Dis."},{"key":"B36","doi-asserted-by":"publisher","first-page":"8076","DOI":"10.1074\/jbc.M109.063388","article-title":"Apical Surface Expression of Aspartic Protease Plasmepsin 4, a Potential Transmission-blocking Target of the Plasmodium Ookinete","volume":"285","author":"Li","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B37","doi-asserted-by":"publisher","first-page":"e29289","DOI":"10.1371\/journal.pone.0029289","article-title":"A novel \u2018gene insertion\/marker out\u2019 (GIMO) method for transgene expression and gene complementation in rodent malaria parasites","volume":"6","author":"Lin","year":"2011","journal-title":"PLoS One"},{"key":"B38","doi-asserted-by":"publisher","first-page":"7703","DOI":"10.1074\/jbc.M115.698282","article-title":"Multiple Plasmodium falciparum Merozoite Surface Protein 1 Complexes Mediate Merozoite Binding to Human Erythrocytes","volume":"291","author":"Lin","year":"2016","journal-title":"J. Biol. Chem."},{"key":"B39","doi-asserted-by":"publisher","first-page":"2098","DOI":"10.1080\/21645515.2017.1295906","article-title":"Efficacy of phase 3 trial of RTS, S\/AS01 malaria vaccine: The need for an alternative development plan","volume":"13","author":"Mahmoudi","year":"2017","journal-title":"Hum. Vaccin. Immunother."},{"key":"B40","doi-asserted-by":"publisher","first-page":"2018","DOI":"10.1128\/IAI.01409-07","article-title":"Murine model for assessment of Plasmodium falciparum transmission-blocking vaccine using transgenic Plasmodium berghei parasites expressing the target antigen Pfs25","volume":"76","author":"Mlambo","year":"2008","journal-title":"Infect. Immun."},{"key":"B41","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1016\/S0140-6736(12)60034-8","article-title":"Global malaria mortality between 1980 and 2010: a systematic analysis","volume":"379","author":"Murray","year":"2012","journal-title":"Lancet"},{"key":"B42","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1042\/bj2350553","article-title":"Calibration of the relative molecular mass of proteoglycan subunit by column chromatography on Sepharose CL-2B","volume":"235","author":"Ohno","year":"1986","journal-title":"Biochem. J."},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2018.00247","article-title":"OX40 Stimulation Enhances Protective Immune Responses Induced After Vaccination With Attenuated Malaria Parasites","volume":"8","author":"Othman","year":"2018","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"e1004120","DOI":"10.1371\/journal.ppat.1004120","article-title":"Multimeric assembly of host-pathogen adhesion complexes involved in apicomplexan invasion","volume":"10","author":"Paing","year":"2014","journal-title":"PLoS Pathog."},{"key":"B45","doi-asserted-by":"publisher","first-page":"412","DOI":"10.4269\/ajtmh.2012.11-0609","article-title":"New ultrastructural analysis of the invasive apparatus of the Plasmodium ookinete","volume":"87","author":"Patra","year":"2012","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"B46","doi-asserted-by":"publisher","first-page":"2492","DOI":"10.1002\/pmic.200700727","article-title":"Proteomic analysis of zygote and ookinete stages of the avian malaria parasite Plasmodium gallinaceum delineates the homologous proteomes of the lethal human malaria parasite Plasmodium falciparum","volume":"8","author":"Patra","year":"2008","journal-title":"Proteomics"},{"key":"B47","doi-asserted-by":"publisher","first-page":"1799","DOI":"10.1128\/IAI.02980-14","article-title":"Alga-produced malaria transmission-blocking vaccine candidate Pfs25 formulated with a human use-compatible potent adjuvant induces high-affinity antibodies that block Plasmodium falciparum infection of mosquitoes","volume":"83","author":"Patra","year":"2015","journal-title":"Infect. Immun."},{"key":"B48","doi-asserted-by":"publisher","first-page":"D442","DOI":"10.1093\/nar\/gky1106","article-title":"The PRIDE database and related tools and resources in 2019: improving support for quantification data","volume":"47","author":"Perez-Riverol","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.1016\/j.ijpara.2011.05.007","article-title":"Vital functions of the malarial ookinete protein, CTRP, reside in the A domains","volume":"41","author":"Ramakrishnan","year":"2011","journal-title":"Int. J. Parasitol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1007\/978-1-4939-2815-6_21","article-title":"Generation of Transgenic Rodent Malaria Parasites Expressing Human Malaria Parasite Proteins","volume":"1325","author":"Salman","year":"2015","journal-title":"Methods Mol. Biol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1007\/978-3-0348-8757-1_16","article-title":"Chitinases of human parasites and their implications as antiparasitic targets","volume":"87","author":"Shahabuddin","year":"1999","journal-title":"EXS"},{"key":"B52","doi-asserted-by":"publisher","first-page":"4266","DOI":"10.1073\/pnas.90.9.4266","article-title":"Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease","volume":"90","author":"Shahabuddin","year":"1993","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B53","doi-asserted-by":"publisher","first-page":"17665","DOI":"10.1074\/jbc.273.28.17665","article-title":"A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization","volume":"273","author":"Shen","year":"1998","journal-title":"J. Biol. Chem."},{"key":"B54","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/0014-4894(91)90132-G","article-title":"The peritrophic membrane as a barrier: its penetration by Plasmodium gallinaceum and the effect of a monoclonal antibody to ookinetes","volume":"72","author":"Sieber","year":"1991","journal-title":"Exp. Parasitol."},{"key":"B55","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/978-94-009-1535-0_7","article-title":"Infection of mosquitoes with rodent malaria","volume-title":"The molecular biology of insect disease vectors","author":"Sinden","year":"1997"},{"key":"B56","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1111\/cmi.12413","article-title":"The cell biology of malaria infection of mosquito: advances and opportunities","volume":"17","author":"Sinden","year":"2015","journal-title":"Cell Microbiol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"e1006336","DOI":"10.1371\/journal.ppat.1006336","article-title":"Developing transmission-blocking strategies for malaria control","volume":"13","author":"Sinden","year":"2017","journal-title":"PLoS Pathog."},{"key":"B58","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/bs.apar.2016.09.004","article-title":"Targeting the Parasite to Suppress Malaria Transmission","volume":"97","author":"Sinden","year":"2017","journal-title":"Adv. Parasitol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/j.pt.2016.09.012","article-title":"Time for Genome Editing: Next-Generation Attenuated Malaria Parasites","volume":"33","author":"Singer","year":"2017","journal-title":"Trends Parasitol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"10311","DOI":"10.1073\/pnas.1409928111","article-title":"Immunization with a functional protein complex required for erythrocyte invasion protects against lethal malaria","volume":"111","author":"Srinivasan","year":"2014","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B61","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1016\/j.parint.2009.05.002","article-title":"Enzymatic characterization of the Plasmodium vivax chitinase, a potential malaria transmission-blocking target","volume":"58","author":"Takeo","year":"2009","journal-title":"Parasitol. Int."},{"key":"B62","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1080\/14760584.2017.1276833","article-title":"Towards clinical development of a Pfs48\/45-based transmission blocking malaria vaccine","volume":"16","author":"Theisen","year":"2017","journal-title":"Expert Rev. Vaccines"},{"key":"B63","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/S0166-6851(03)00140-3","article-title":"Gene structure and ookinete expression of the chitinase genes of Plasmodium vivax and Plasmodium yoelii","volume":"130","author":"Tsuboi","year":"2003","journal-title":"Mol. Biochem. Parasitol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"1403","DOI":"10.1038\/s41564-017-0007-4","article-title":"Hexahydroquinolines are antimalarial candidates with potent blood-stage and transmission-blocking activity","volume":"2","author":"Vanaerschot","year":"2017","journal-title":"Nat. Microbiol."},{"key":"B65","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2015.09.074","article-title":"Workshop report: Malaria vaccine development in Europe-preparing for the future","volume":"2015","author":"Viebig","year":"2015","journal-title":"Vaccine"},{"key":"B66","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1006\/expr.1998.4322","article-title":"Plasmodium gallinaceum: use of antisera to degenerate synthetic peptides derived from the active site of protozoal chitinases to characterize an ookinete-specific chitinase","volume":"90","author":"Vinetz","year":"1998","journal-title":"Exp. Parasitol."},{"key":"B67","doi-asserted-by":"publisher","first-page":"14061","DOI":"10.1073\/pnas.96.24.14061","article-title":"The chitinase PfCHT1 from the human malaria parasite Plasmodium falciparum lacks proenzyme and chitin-binding domains and displays unique substrate preferences","volume":"96","author":"Vinetz","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B68","doi-asserted-by":"publisher","first-page":"10331","DOI":"10.1074\/jbc.275.14.10331","article-title":"Chitinases of the avian malaria parasite Plasmodium gallinaceum, a class of enzymes necessary for parasite invasion of the mosquito midgut","volume":"275","author":"Vinetz","year":"2000","journal-title":"J. Biol. Chem."},{"key":"B69","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1007\/3-540-29088-5_14","article-title":"Plasmodium ookinete invasion of the mosquito midgut","volume":"295","author":"Vinetz","year":"2005","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"B70","doi-asserted-by":"publisher","first-page":"5195","DOI":"10.1093\/emboj\/18.19.5195","article-title":"The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands","volume":"18","author":"Wengelnik","year":"1999","journal-title":"EMBO J."},{"key":"B71","doi-asserted-by":"publisher","first-page":"e1003943","DOI":"10.1371\/journal.ppat.1003943","article-title":"Plasmodium falciparum erythrocyte invasion: combining function with immune evasion","volume":"10","author":"Wright","year":"2014","journal-title":"PLoS Pathog."},{"key":"B72","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.molbiopara.2016.12.010","article-title":"CRISPR\/Cas9 mediated sequential editing of genes critical for ookinete motility in Plasmodium yoelii","volume":"212","author":"Zhang","year":"2017","journal-title":"Mol. Biochem. Parasitol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2020.615343\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,14]],"date-time":"2021-01-14T02:28:36Z","timestamp":1610591316000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2020.615343\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,8]]},"references-count":72,"alternative-id":["10.3389\/fcimb.2020.615343"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2020.615343","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,8]]},"article-number":"615343"}}