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Article ; Online: Variable long-term protection by radiation-, chemo-, and genetically-attenuated Plasmodium berghei sporozoite vaccines.

Moita, Diana / Nunes-Cabaço, Helena / Rôla, Catarina / Franke-Fayard, Blandine / Janse, Chris J / Mendes, António M / Prudêncio, Miguel

Vaccine

2023 Volume 41, Issue 51, Page(s) 7618–7625

Abstract: Long-term protection against malaria remains one of the greatest challenges of vaccination against this deadly parasitic disease. Whole-sporozoite (WSp) malaria vaccine formulations, which target the Plasmodium parasite's pre-erythrocytic stages, include ...

Abstract	Long-term protection against malaria remains one of the greatest challenges of vaccination against this deadly parasitic disease. Whole-sporozoite (WSp) malaria vaccine formulations, which target the Plasmodium parasite's pre-erythrocytic stages, include radiation-attenuated sporozoites (RAS), early- and late-arresting genetically-attenuated parasites (EA-GAP and LA-GAP, respectively), and chemoprophylaxis with sporozoites (CPS). Although all these four vaccine formulations induce protective immune responses in the clinic, data on the longevity of the antimalarial protection they afford remain scarce. We employed a mouse model of malaria to assess protection conferred by immunization with P. berghei (Pb)-based surrogates of these four WSp formulations over a 36-week period. We show that EA-GAP WSp provide the lowest overall protection against an infectious Pb challenge, and that while immunization with RAS and LA-GAP WSp elicits the most durable protection, the protective efficacy of CPS WSp wanes rapidly over the 36-week period, most notably at higher immunization dosages. Analyses of liver immune cells show that CD44
MeSH term(s)	Humans ; Animals ; Mice ; Plasmodium berghei/genetics ; Sporozoites ; Vaccines, Attenuated ; CD8-Positive T-Lymphocytes ; Lead ; Malaria ; Malaria Vaccines
Chemical Substances	Vaccines, Attenuated ; Lead (2P299V784P) ; Malaria Vaccines
Language	English
Publishing date	2023-11-25
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	605674-x
ISSN	1873-2518 ; 0264-410X
ISSN (online)	1873-2518
ISSN	0264-410X
DOI	10.1016/j.vaccine.2023.11.023
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Article ; Online: Streamlining sporozoite isolation from mosquitoes by leveraging the dynamics of migration to the salivary glands.

Pathak, Ashutosh K / Shiau, Justine C / Franke-Fayard, Blandine / Shollenberger, Lisa M / Harn, Donald A / Kyle, Dennis E / Murdock, Courtney C

Malaria journal

2022 Volume 21, Issue 1, Page(s) 264

Abstract: Background: Sporozoites isolated from the salivary glands of Plasmodium-infected mosquitoes are a prerequisite for several basic and pre-clinical applications. Although salivary glands are pooled to maximize sporozoite recovery, insufficient yields pose ...

Abstract	Background: Sporozoites isolated from the salivary glands of Plasmodium-infected mosquitoes are a prerequisite for several basic and pre-clinical applications. Although salivary glands are pooled to maximize sporozoite recovery, insufficient yields pose logistical and analytical hurdles; thus, predicting yields prior to isolation would be valuable. Preceding oocyst densities in the midgut is an obvious candidate. However, it is unclear whether current understanding of its relationship with sporozoite densities can be used to maximize yields, or whether it can capture the potential density-dependence in rates of sporozoite invasion of the salivary glands. Methods: This study presents a retrospective analysis of Anopheles stephensi mosquitoes infected with two strains of the rodent-specific Plasmodium berghei. Mean oocyst densities were estimated in the midguts earlier in the infection (11-15 days post-blood meal), with sporozoites pooled from the salivary glands later in the infection (17-29 days). Generalized linear mixed effects models were used to determine if (1) mean oocyst densities can predict sporozoite yields from pooled salivary glands, (2) whether these densities can capture differences in rates of sporozoite invasion of salivary glands, and (3), if the interaction between oocyst densities and time could be leveraged to boost overall yields. Results: The non-linear effect of mean oocyst densities confirmed the role of density-dependent constraints in limiting yields beyond certain oocyst densities. Irrespective of oocyst densities however, the continued invasion of salivary glands by the sporozoites boosted recoveries over time (17-29 days post-blood meal) for either parasite strain. Conclusions: Sporozoite invasion of the salivary glands over time can be leveraged to maximize yields for P. berghei. In general, however, invasion of the salivary glands over time is a critical fitness determinant for all Plasmodium species (extrinsic incubation period, EIP). Thus, delaying sporozoite collection could, in principle, substantially reduce dissection effort for any parasite within the genus, with the results also alluding to the potential for changes in sporozoites densities over time to modify infectivity for the next host.
MeSH term(s)	Animals ; Anopheles/parasitology ; Plasmodium berghei ; Retrospective Studies ; Salivary Glands/parasitology ; Sporozoites
Language	English
Publishing date	2022-09-13
Publishing country	England
Document type	Journal Article
ZDB-ID	2091229-8
ISSN	1475-2875 ; 1475-2875
ISSN (online)	1475-2875
ISSN	1475-2875
DOI	10.1186/s12936-022-04270-y
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Article ; Online: The effect of dosage on the protective efficacy of whole-sporozoite formulations for immunization against malaria.

Moita, Diana / Rôla, Catarina / Nunes-Cabaço, Helena / Nogueira, Gonçalo / Maia, Teresa G / Othman, Ahmad Syibli / Franke-Fayard, Blandine / Janse, Chris J / Mendes, António M / Prudêncio, Miguel

NPJ vaccines

2023 Volume 8, Issue 1, Page(s) 182

Abstract: Immunization with Plasmodium sporozoites, either attenuated or administered under the cover of an antimalarial drug, can induce strong protection against malaria in pre-clinical murine models, as well as in human trials. Previous studies have suggested ... ...

Abstract	Immunization with Plasmodium sporozoites, either attenuated or administered under the cover of an antimalarial drug, can induce strong protection against malaria in pre-clinical murine models, as well as in human trials. Previous studies have suggested that whole-sporozoite (WSpz) formulations based on parasites with longer liver stage development induce higher protection, but a comparative analysis of four different WSpz formulations has not been reported. We employed a rodent model of malaria to analyze the effect of immunization dosage on the protective efficacy of WSpz formulations consisting of (i) early liver arresting genetically attenuated parasites (EA-GAP) or (ii) radiation-attenuated sporozoites (RAS), (iii) late arresting GAP (LA-GAP), and (iv) sporozoites administered under chemoprophylaxis, that are eliminated upon release into the bloodstream (CPS). Our results show that, unlike all other WSpz formulations, EA-GAP fails to confer complete protection against an infectious challenge at any immunization dosage employed, suggesting that a minimum threshold of liver development is required to elicit fully effective immune responses. Moreover, while immunization with RAS, LA-GAP and CPS WSpz yields comparable, dosage-dependent protection, protection by EA-GAP WSpz peaks at an intermediate dosage and markedly decreases thereafter. In-depth immunological analyses suggest that effector CD8+ T cells elicited by EA-GAP WSpz immunization have limited developmental plasticity, with a potential negative impact on the functional versatility of memory cells and, thus, on protective immunity. Our findings point towards dismissing EA-GAP from prioritization for WSpz malaria vaccination and enhance our understanding of the complexity of the protection elicited by these WSpz vaccine candidates, guiding their future optimization.
Language	English
Publishing date	2023-11-24
Publishing country	England
Document type	Journal Article
ISSN	2059-0105
ISSN (online)	2059-0105
DOI	10.1038/s41541-023-00778-9
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Article ; Online: A versatile Plasmodium falciparum reporter line expressing NanoLuc enables highly sensitive multi-stage drug assays.

Miyazaki, Yukiko / Vos, Martijn W / Geurten, Fiona J A / Bigeard, Pierre / Kroeze, Hans / Yoshioka, Shohei / Arisawa, Mitsuhiro / Inaoka, Daniel Ken / Soulard, Valerie / Dechering, Koen J / Franke-Fayard, Blandine / Miyazaki, Shinya

Communications biology

2023 Volume 6, Issue 1, Page(s) 713

Abstract: Transgenic luciferase-expressing Plasmodium falciparum parasites have been widely used for the evaluation of anti-malarial compounds. Here, to screen for anti-malarial drugs effective against multiple stages of the parasite, we generate a P. falciparum ... ...

Abstract	Transgenic luciferase-expressing Plasmodium falciparum parasites have been widely used for the evaluation of anti-malarial compounds. Here, to screen for anti-malarial drugs effective against multiple stages of the parasite, we generate a P. falciparum reporter parasite that constitutively expresses NanoLuciferase (NanoLuc) throughout its whole life cycle. The NanoLuc-expressing P. falciparum reporter parasite shows a quantitative NanoLuc signal in the asexual blood, gametocyte, mosquito, and liver stages. We also establish assay systems to evaluate the anti-malarial activity of compounds at the asexual blood, gametocyte, and liver stages, and then determine the 50% inhibitory concentration (IC
MeSH term(s)	Humans ; Animals ; Antimalarials/pharmacology ; Plasmodium falciparum/genetics ; Animals, Genetically Modified ; Biological Assay
Chemical Substances	nanoluc (EC 1.13.12.-) ; Antimalarials
Language	English
Publishing date	2023-07-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-023-05078-5
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Article ; Online: Ageing of Plasmodium falciparum malaria sporozoites alters their motility, infectivity and reduces immune activation in vitro.

van Schuijlenburg, Roos / Azargoshasb, Samaneh / de Korne, Clarize M / Sijtsma, Jeroen C / Bezemer, Sascha / van der Ham, Alwin J / Baalbergen, Els / Geurten, Fiona / de Bes-Roeleveld, Laura M / Chevalley-Maurel, Severine C / van Oosterom, Matthias N / van Leeuwen, Fijs W B / Franke-Fayard, Blandine / Roestenberg, Meta

Malaria journal

2024 Volume 23, Issue 1, Page(s) 111

Abstract: Background: Sporozoites (SPZ), the infective form of Plasmodium falciparum malaria, can be inoculated into the human host skin by Anopheline mosquitoes. These SPZ migrate at approximately 1 µm/s to find a blood vessel and travel to the liver where they ... ...

Abstract	Background: Sporozoites (SPZ), the infective form of Plasmodium falciparum malaria, can be inoculated into the human host skin by Anopheline mosquitoes. These SPZ migrate at approximately 1 µm/s to find a blood vessel and travel to the liver where they infect hepatocytes and multiply. In the skin they are still low in number (50-100 SPZ) and vulnerable to immune attack by antibodies and skin macrophages. This is why whole SPZ and SPZ proteins are used as the basis for most malaria vaccines currently deployed and undergoing late clinical testing. Mosquitoes typically inoculate SPZ into a human host between 14 and 25 days after their previous infective blood meal. However, it is unknown whether residing time within the mosquito affects SPZ condition, infectivity or immunogenicity. This study aimed to unravel how the age of P. falciparum SPZ in salivary glands (14, 17, or 20 days post blood meal) affects their infectivity and the ensuing immune responses. Methods: SPZ numbers, viability by live/dead staining, motility using dedicated sporozoite motility orienting and organizing tool software (SMOOT), and infectivity of HC-04.j7 liver cells at 14, 17 and 20 days after mosquito feeding have been investigated. In vitro co-culture assays with SPZ stimulated monocyte-derived macrophages (MoMɸ) and CD8 Results: SPZ age did not result in different SPZ numbers or viability. However, a markedly different motility pattern, whereby motility decreased from 89% at day 14 to 80% at day 17 and 71% at day 20 was observed (p ≤ 0.0001). Similarly, infectivity of day 20 SPZ dropped to ~ 50% compared with day 14 SPZ (p = 0.004). MoMɸ were better able to take up day 14 SPZ than day 20 SPZ (from 7.6% to 4.1%, p = 0.03) and displayed an increased expression of pro-inflammatory CD80, IL-6 (p = 0.005), regulatory markers PDL1 (p = 0.02), IL-10 (p = 0.009) and cytokines upon phagocytosis of younger SPZ. Interestingly, co-culture of these cells with CD8 Conclusion: Overall, this data is a first step in enhancing the understanding of how mosquito residing time affects P. falciparum SPZ and could impact the understanding of the P. falciparum infectious reservoir and the potency of whole SPZ vaccines.
MeSH term(s)	Animals ; Humans ; Sporozoites ; CD8-Positive T-Lymphocytes ; Malaria, Falciparum ; Malaria Vaccines ; Culicidae ; Aging ; Plasmodium falciparum
Chemical Substances	Malaria Vaccines
Language	English
Publishing date	2024-04-19
Publishing country	England
Document type	Journal Article
ZDB-ID	2091229-8
ISSN	1475-2875 ; 1475-2875
ISSN (online)	1475-2875
ISSN	1475-2875
DOI	10.1186/s12936-024-04946-7
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Article ; Online: Author Correction: Glycosylated nanoparticle-based PfCSP vaccine confers long-lasting antibody responses and sterile protection in mouse malaria model.

Ludwig, Julia / Scally, Stephen W / Costa, Giulia / Hoffmann, Sandro / Murugan, Rajagopal / Lossin, Jana / Prieto, Katherine / Obraztsova, Anna / Lobeto, Nina / Franke-Fayard, Blandine / Janse, Chris J / Lebas, Celia / Collin, Nicolas / Binter, Spela / Kellam, Paul / Levashina, Elena A / Wardemann, Hedda / Julien, Jean-Philippe

NPJ vaccines

2023 Volume 8, Issue 1, Page(s) 86

Language	English
Publishing date	2023-06-05
Publishing country	England
Document type	Published Erratum
ISSN	2059-0105
ISSN (online)	2059-0105
DOI	10.1038/s41541-023-00687-x
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Article ; Online: Glycosylated nanoparticle-based PfCSP vaccine confers long-lasting antibody responses and sterile protection in mouse malaria model.

NPJ vaccines

2023 Volume 8, Issue 1, Page(s) 52

Abstract: The development of an effective and durable vaccine remains a central goal in the fight against malaria. Circumsporozoite protein (CSP) is the major surface protein of sporozoites and the target of the only licensed Plasmodium falciparum (Pf) malaria ... ...

Abstract	The development of an effective and durable vaccine remains a central goal in the fight against malaria. Circumsporozoite protein (CSP) is the major surface protein of sporozoites and the target of the only licensed Plasmodium falciparum (Pf) malaria vaccine, RTS,S/AS01. However, vaccine efficacy is low and short-lived, highlighting the need for a second-generation vaccine with superior efficacy and durability. Here, we report a Helicobacter pylori apoferritin-based nanoparticle immunogen that elicits strong B cell responses against PfCSP epitopes that are targeted by the most potent human monoclonal antibodies. Glycan engineering of the scaffold and fusion of an exogenous T cell epitope enhanced the anti-PfCSP B cell response eliciting strong, long-lived and protective humoral immunity in mice. Our study highlights the power of rational vaccine design to generate a highly efficacious second-generation anti-infective malaria vaccine candidate and provides the basis for its further development.
Language	English
Publishing date	2023-04-07
Publishing country	England
Document type	Journal Article
ISSN	2059-0105
ISSN (online)	2059-0105
DOI	10.1038/s41541-023-00653-7
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Article ; Online: Chemically augmented malaria sporozoites display an altered immunogenic profile.

Duszenko, Nikolas / van Schuijlenburg, Roos / Chevalley-Maurel, Severine / van Willigen, Danny M / de Bes-Roeleveld, Laura / van der Wees, Stefanie / Naar, Chanel / Baalbergen, Els / Heieis, Graham / Bunschoten, Anton / Velders, Aldrik H / Franke-Fayard, Blandine / van Leeuwen, Fijs W B / Roestenberg, Meta

Frontiers in immunology

2023 Volume 14, Page(s) 1204606

Abstract: Despite promising results in malaria-naïve individuals, whole sporozoite (SPZ) vaccine efficacy in malaria-endemic settings has been suboptimal. Vaccine hypo-responsiveness due to previous malaria exposure has been posited as responsible, indicating the ... ...

Abstract	Despite promising results in malaria-naïve individuals, whole sporozoite (SPZ) vaccine efficacy in malaria-endemic settings has been suboptimal. Vaccine hypo-responsiveness due to previous malaria exposure has been posited as responsible, indicating the need for SPZ vaccines of increased immunogenicity. To this end, we here demonstrate a proof-of-concept for altering SPZ immunogenicity, where supramolecular chemistry enables chemical augmentation of the parasite surface with a TLR7 agonist-based adjuvant (SPZ-SAS(CL307)).
MeSH term(s)	Animals ; Mice ; CD8-Positive T-Lymphocytes ; Sporozoites ; Malaria/prevention & control ; Malaria Vaccines ; Adjuvants, Immunologic
Chemical Substances	Malaria Vaccines ; Adjuvants, Immunologic
Language	English
Publishing date	2023-08-31
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1204606
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Article ; Online: Plasmodium berghei sporozoites in nonreplicative vacuole are eliminated by a PI3P-mediated autophagy-independent pathway.

Bindschedler, Annina / Wacker, Rahel / Egli, Jessica / Eickel, Nina / Schmuckli-Maurer, Jacqueline / Franke-Fayard, Blandine M / Janse, Chris J / Heussler, Volker T

Cellular microbiology

2020 Volume 23, Issue 1, Page(s) e13271

Abstract: The protozoan parasite Plasmodium, causative agent of malaria, invades hepatocytes by invaginating the host cell plasma membrane and forming a parasitophorous vacuole membrane (PVM). Surrounded by this PVM, the parasite undergoes extensive replication. ... ...

Abstract	The protozoan parasite Plasmodium, causative agent of malaria, invades hepatocytes by invaginating the host cell plasma membrane and forming a parasitophorous vacuole membrane (PVM). Surrounded by this PVM, the parasite undergoes extensive replication. Parasites inside a PVM provoke the Plasmodium-associated autophagy-related (PAAR) response. This is characterised by a long-lasting association of the autophagy marker protein LC3 with the PVM, which is not preceded by phosphatidylinositol 3-phosphate (PI3P)-labelling. Prior to productive invasion, sporozoites transmigrate several cells and here we describe that a proportion of traversing sporozoites become trapped in a transient traversal vacuole, provoking a host cell response that clearly differs from the PAAR response. These trapped sporozoites provoke PI3P-labelling of the surrounding vacuolar membrane immediately after cell entry, followed by transient LC3-labelling and elimination of the parasite by lysosomal acidification. Our data suggest that this PI3P response is not only restricted to sporozoites trapped during transmigration but also affects invaded parasites residing in a compromised vacuole. Thus, host cells can employ a pathway distinct from the previously described PAAR response to efficiently recognise and eliminate Plasmodium parasites.
MeSH term(s)	Animals ; Autophagy ; Cell Line ; Female ; HeLa Cells ; Hepatocytes/parasitology ; Host-Parasite Interactions ; Humans ; Malaria/parasitology ; Mice ; Microtubule-Associated Proteins/metabolism ; Organisms, Genetically Modified ; Phosphatidylinositol Phosphates/metabolism ; Plasmodium berghei/metabolism ; Plasmodium berghei/parasitology ; Sporozoites/metabolism ; Vacuoles/parasitology
Chemical Substances	MAP1LC3A protein, human ; Microtubule-Associated Proteins ; Phosphatidylinositol Phosphates ; phosphatidylinositol 3-phosphate
Language	English
Publishing date	2020-10-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1468320-9
ISSN	1462-5822 ; 1462-5814
ISSN (online)	1462-5822
ISSN	1462-5814
DOI	10.1111/cmi.13271
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Zs.A 5288: Show issues

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Article ; Online: Suppression of Plasmodium MIF-CD74 signaling protects against severe malaria.

Baeza Garcia, Alvaro / Siu, Edwin / Du, Xin / Leng, Lin / Franke-Fayard, Blandine / Janse, Chris J / Howland, Shanshan W / Rénia, Laurent / Lolis, Elias / Bucala, Richard

FASEB journal : official publication of the Federation of American Societies for Experimental Biology

2021 Volume 35, Issue 12, Page(s) e21997

Abstract: The deadliest complication of infection by Plasmodium parasites, cerebral malaria, accounts for the majority of malarial fatalities. Although our understanding of the cellular and molecular mechanisms underlying the pathology remains incomplete, recent ... ...

Abstract	The deadliest complication of infection by Plasmodium parasites, cerebral malaria, accounts for the majority of malarial fatalities. Although our understanding of the cellular and molecular mechanisms underlying the pathology remains incomplete, recent studies support the contribution of systemic and neuroinflammation as the cause of cerebral edema and blood-brain barrier (BBB) dysfunction. All Plasmodium species encode an orthologue of the innate cytokine, Macrophage Migration Inhibitory Factor (MIF), which functions in mammalian biology to regulate innate responses. Plasmodium MIF (PMIF) similarly signals through the host MIF receptor CD74, leading to an enhanced inflammatory response. We investigated the PMIF-CD74 interaction in the onset of experimental cerebral malaria (ECM) and liver stage Plasmodium development by using a combination of CD74 deficient (Cd74
MeSH term(s)	Animals ; Antigens, Differentiation, B-Lymphocyte/chemistry ; Antigens, Differentiation, B-Lymphocyte/physiology ; CD8-Positive T-Lymphocytes/immunology ; Histocompatibility Antigens Class II/chemistry ; Histocompatibility Antigens Class II/physiology ; Inflammation/etiology ; Inflammation/metabolism ; Inflammation/pathology ; Inflammation/prevention & control ; Liver/immunology ; Liver/parasitology ; Liver/pathology ; Macrophage Migration-Inhibitory Factors/antagonists & inhibitors ; Macrophage Migration-Inhibitory Factors/metabolism ; Malaria, Cerebral/etiology ; Malaria, Cerebral/metabolism ; Malaria, Cerebral/pathology ; Malaria, Cerebral/prevention & control ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Plasmodium berghei/physiology
Chemical Substances	Antigens, Differentiation, B-Lymphocyte ; Histocompatibility Antigens Class II ; Macrophage Migration-Inhibitory Factors ; invariant chain
Language	English
Publishing date	2021-10-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	639186-2
ISSN	1530-6860 ; 0892-6638
ISSN (online)	1530-6860
ISSN	0892-6638
DOI	10.1096/fj.202101072R
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