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However, there are limited studies assessing whether combining human mAbs against distinct regions of the<jats:italic>Plasmodium falciparum<\/jats:italic>(Pf) circumsporozoite protein (CSP) enhances<jats:italic>in vivo<\/jats:italic>protection against malaria compared to each mAb alone or whether passive transfer of PfCSP mAbs would improve protection following vaccination against PfCSP. Here, we isolated a panel of human mAbs against the subdominant C-terminal domain of PfCSP (C-CSP) from a volunteer immunized with radiation-attenuated Pf sporozoites. These C-CSP-specific mAbs had limited binding to sporozoites<jats:italic>in vitro<\/jats:italic>that was increased by combination with neutralizing human \u201crepeat\u201d mAbs against the NPDP\/NVDP\/NANP tetrapeptides in the central repeat region of PfCSP. Nevertheless, passive transfer of repeat- and C-CSP-specific mAb combinations did not provide enhanced protection against<jats:italic>in vivo<\/jats:italic>sporozoite challenge compared to repeat mAbs alone. Furthermore, combining potent repeat-specific mAbs (CIS43, L9, and 317) that respectively target the three tetrapeptides (NPDP\/NVDP\/NANP) did not provide additional protection against<jats:italic>in vivo<\/jats:italic>sporozoite challenge. However, administration of either CIS43, L9, or 317 (but not C-CSP-specific mAbs) to mice that had been immunized with R21, a PfCSP-based virus-like particle vaccine that induces polyclonal antibodies against the repeat region and C-CSP, provided enhanced protection against sporozoite challenge when compared to vaccine or mAbs alone. Collectively, this study shows that while combining mAbs against the repeat and C-terminal regions of PfCSP provide no additional protection<jats:italic>in vivo<\/jats:italic>, repeat mAbs do provide increased protection when combined with vaccine-induced polyclonal antibodies. These data should inform the implementation of PfCSP human mAbs alone or following vaccination to prevent malaria infection.<\/jats:p>","DOI":"10.1371\/journal.ppat.1010133","type":"journal-article","created":{"date-parts":[[2021,12,6]],"date-time":"2021-12-06T18:30:28Z","timestamp":1638815428000},"page":"e1010133","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":39,"title":["Protective effects of combining monoclonal antibodies and vaccines against the Plasmodium falciparum circumsporozoite protein"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8026-8044","authenticated-orcid":true,"given":"Lawrence T.","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9112-3377","authenticated-orcid":true,"given":"Lais S.","family":"Pereira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3257-5920","authenticated-orcid":true,"given":"Patience K.","family":"Kiyuka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2015-2090","authenticated-orcid":true,"given":"Arne","family":"Sch\u00f6n","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neville K.","family":"Kisalu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachel","family":"Vistein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8670-5487","authenticated-orcid":true,"given":"Marlon","family":"Dillon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4067-7476","authenticated-orcid":true,"given":"Brian G.","family":"Bonilla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5137-4836","authenticated-orcid":true,"given":"Alvaro","family":"Molina-Cruz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carolina","family":"Barillas-Mury","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6661-6372","authenticated-orcid":true,"given":"Joshua","family":"Tan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1847-5488","authenticated-orcid":true,"given":"Azza H.","family":"Idris","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1336-4682","authenticated-orcid":true,"given":"Joseph R.","family":"Francica","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3133-0849","authenticated-orcid":true,"given":"Robert A.","family":"Seder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,12,6]]},"reference":[{"key":"ppat.1010133.ref001","unstructured":"WHO. 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Triller","year":"2017","journal-title":"Immunity"},{"key":"ppat.1010133.ref019","article-title":"Evolution of protective human antibodies against Plasmodium falciparum circumsporozoite protein repeat motifs","author":"R Murugan","year":"2020","journal-title":"Nat Med"},{"issue":"4","key":"ppat.1010133.ref020","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1038\/nm.4513","article-title":"A public antibody lineage that potently inhibits malaria infection through dual binding to the circumsporozoite protein","volume":"24","author":"J Tan","year":"2018","journal-title":"Nat Med"},{"issue":"4","key":"ppat.1010133.ref021","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1038\/nm.4512","article-title":"A human monoclonal antibody prevents malaria infection by targeting a new site of vulnerability on the parasite","volume":"24","author":"NK Kisalu","year":"2018","journal-title":"Nat Med"},{"issue":"2","key":"ppat.1010133.ref022","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1084\/jem.20101488","article-title":"The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host","volume":"208","author":"A Coppi","year":"2011","journal-title":"J Exp Med"},{"issue":"17","key":"ppat.1010133.ref023","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1016\/0161-5890(95)00136-0","article-title":"Synthesis and immunological characterization of 104-mer and 102-mer peptides corresponding to the N- and C-terminal regions of the Plasmodium falciparum CS protein","volume":"32","author":"MA Roggero","year":"1995","journal-title":"Molecular Immunology"},{"key":"ppat.1010133.ref024","doi-asserted-by":"crossref","DOI":"10.1186\/s12936-016-1348-9","article-title":"The biological function of antibodies induced by the RTS,S\/AS01 malaria vaccine candidate is determined by their fine specificity","volume":"15","author":"S Chaudhury","year":"2016","journal-title":"Malar J"},{"issue":"1","key":"ppat.1010133.ref025","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1186\/s12916-019-1277-x","article-title":"Induction and decay of functional complement-fixing antibodies by the RTS,S malaria vaccine in children, and a negative impact of malaria exposure","volume":"17","author":"L Kurtovic","year":"2019","journal-title":"BMC Med"},{"issue":"1","key":"ppat.1010133.ref026","doi-asserted-by":"crossref","first-page":"2174","DOI":"10.1038\/s41467-019-10195-z","article-title":"Concentration and avidity of antibodies to different circumsporozoite epitopes correlate with RTS,S\/AS01E malaria vaccine efficacy","volume":"10","author":"C Doba\u00f1o","year":"2019","journal-title":"Nat Commun"},{"key":"ppat.1010133.ref027","article-title":"Breadth of humoral immune responses to the C-terminus of the circumsporozoite protein is associated with protective efficacy induced by the RTS,S malaria vaccine","author":"S Chaudhury","year":"2021","journal-title":"Vaccine"},{"issue":"1","key":"ppat.1010133.ref028","doi-asserted-by":"crossref","first-page":"7998","DOI":"10.1038\/s41598-017-08526-5","article-title":"Delayed fractional dose regimen of the RTS,S\/AS01 malaria vaccine candidate enhances an IgG4 response that inhibits serum opsonophagocytosis","volume":"7","author":"S Chaudhury","year":"2017","journal-title":"Sci Rep"},{"issue":"1","key":"ppat.1010133.ref029","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1186\/s12916-018-1186-4","article-title":"Baseline exposure, antibody subclass, and hepatitis B response differentially affect malaria protective immunity following RTS,S\/AS01E vaccination in African children","volume":"16","author":"I Ubillos","year":"2018","journal-title":"BMC Med"},{"issue":"21","key":"ppat.1010133.ref030","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1056\/NEJMoa1505819","article-title":"Genetic Diversity and Protective Efficacy of the RTS,S\/AS01 Malaria Vaccine","volume":"373","author":"DE Neafsey","year":"2015","journal-title":"N Engl J Med"},{"issue":"1","key":"ppat.1010133.ref031","doi-asserted-by":"crossref","first-page":"6622","DOI":"10.1038\/s41598-018-24585-8","article-title":"RTS,S\/AS01 malaria vaccine mismatch observed among Plasmodium falciparum isolates from southern and central Africa and globally","volume":"8","author":"JC Pringle","year":"2018","journal-title":"Sci Rep"},{"issue":"1","key":"ppat.1010133.ref032","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1084\/jem.20170869","article-title":"Rare PfCSP C-terminal antibodies induced by live sporozoite vaccination are ineffective against malaria infection","volume":"215","author":"SW Scally","year":"2018","journal-title":"J Exp Med"},{"issue":"10","key":"ppat.1010133.ref033","doi-asserted-by":"crossref","first-page":"3771","DOI":"10.1128\/IAI.02676-14","article-title":"Reversible Conformational Change in the Plasmodium falciparum Circumsporozoite Protein Masks Its Adhesion Domains","volume":"83","author":"R Herrera","year":"2015","journal-title":"Infection and Immunity"},{"issue":"6","key":"ppat.1010133.ref034","doi-asserted-by":"crossref","first-page":"2110","DOI":"10.1074\/jbc.M116.754796","article-title":"Force Spectroscopy of the Plasmodium falciparum Vaccine Candidate Circumsporozoite Protein Suggests a Mechanically Pliable Repeat Region","volume":"292","author":"AP Patra","year":"2017","journal-title":"J Biol Chem"},{"issue":"39","key":"ppat.1010133.ref035","doi-asserted-by":"crossref","first-page":"26951","DOI":"10.1074\/jbc.M109.013706","article-title":"Structure of the Plasmodium falciparum circumsporozoite protein, a leading malaria vaccine candidate","volume":"284","author":"ML Plassmeyer","year":"2009","journal-title":"J Biol Chem"},{"issue":"6916","key":"ppat.1010133.ref036","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1038\/nature01188","article-title":"HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites","volume":"420","author":"PD Kwong","year":"2002","journal-title":"Nature"},{"issue":"7724","key":"ppat.1010133.ref037","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1038\/s41586-018-0531-2","article-title":"Combination therapy with anti-HIV-1 antibodies maintains viral suppression","volume":"561","author":"P Mendoza","year":"2018","journal-title":"Nature"},{"key":"ppat.1010133.ref038","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.virol.2014.11.011","article-title":"Complementary and synergistic activities of anti-V3, CD4bs and CD4i antibodies derived from a single individual can cover a wide range of HIV-1 strains","volume":"475","author":"KP Ramirez Valdez","year":"2015","journal-title":"Virology"},{"key":"ppat.1010133.ref039","doi-asserted-by":"crossref","first-page":"46621","DOI":"10.1038\/srep46621","article-title":"Enhancing protective immunity to malaria with a highly immunogenic virus-like particle vaccine","volume":"7","author":"KA Collins","year":"2017","journal-title":"Sci Rep"},{"key":"ppat.1010133.ref040","article-title":"A Potent Anti-Malarial Human Monoclonal Antibody Targets Circumsporozoite Protein Minor Repeats and Neutralizes Sporozoites in the Liver","author":"LT Wang","year":"2020","journal-title":"Immunity"},{"issue":"6395","key":"ppat.1010133.ref041","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1126\/science.aar5304","article-title":"Antihomotypic affinity maturation improves human B cell responses against a repetitive epitope","volume":"360","author":"K Imkeller","year":"2018","journal-title":"Science"},{"issue":"1","key":"ppat.1010133.ref042","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/0022-2836(92)90699-K","article-title":"Molecular basis of co-operativity in protein folding. III. Structural identification of cooperative folding units and folding intermediates","volume":"227","author":"KP Murphy","year":"1992","journal-title":"J Mol Biol"},{"issue":"4","key":"ppat.1010133.ref043","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1002\/prot.340220410","article-title":"The heat capacity of proteins","volume":"22","author":"J G\u00f3mez","year":"1995","journal-title":"Proteins"},{"issue":"48","key":"ppat.1010133.ref044","doi-asserted-by":"crossref","first-page":"E10438","DOI":"10.1073\/pnas.1715812114","article-title":"Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein","volume":"114","author":"D Oyen","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"issue":"10","key":"ppat.1010133.ref045","doi-asserted-by":"crossref","first-page":"eaau8529","DOI":"10.1126\/sciadv.aau8529","article-title":"Cryo-EM structure of P. falciparum circumsporozoite protein with a vaccine-elicited antibody is stabilized by somatically mutated inter-Fab contacts","volume":"4","author":"D Oyen","year":"2018","journal-title":"Sci Adv"},{"issue":"1","key":"ppat.1010133.ref046","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1084\/jem.20040989","article-title":"The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion","volume":"201","author":"A Coppi","year":"2005","journal-title":"J Exp Med"},{"issue":"11","key":"ppat.1010133.ref047","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1038\/s41564-018-0254-z","article-title":"Cytotoxic anti-circumsporozoite antibodies target malaria sporozoites in the host skin","volume":"3","author":"E Aliprandini","year":"2018","journal-title":"Nat Microbiol."},{"issue":"6","key":"ppat.1010133.ref048","doi-asserted-by":"crossref","first-page":"e02194","DOI":"10.1128\/mBio.02194-18","article-title":"Antibody-Mediated Protection against Plasmodium Sporozoites Begins at the Dermal Inoculation 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