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      Sequential Membrane Rupture and Vesiculation during Plasmodium berghei Gametocyte Egress from the Red Blood Cell

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          Abstract

          Malaria parasites alternate between intracellular and extracellular stages and successful egress from the host cell is crucial for continuation of the life cycle. We investigated egress of Plasmodium berghei gametocytes, an essential process taking place within a few minutes after uptake of a blood meal by the mosquito. Egress entails the rupture of two membranes surrounding the parasite: the parasitophorous vacuole membrane (PVM), and the red blood cell membrane (RBCM). High-speed video microscopy of 56 events revealed that egress in both genders comprises four well-defined phases, although each event is slightly different. The first phase is swelling of the host cell, followed by rupture and immediate vesiculation of the PVM. These vesicles are extruded through a single stabilized pore of the RBCM, and the latter is subsequently vesiculated releasing the free gametes. The time from PVM vesiculation to completion of egress varies between events. These observations were supported by immunofluorescence microscopy using antibodies against proteins of the RBCM and PVM. The combined results reveal dynamic re-organization of the membranes and the cortical cytoskeleton of the erythrocyte during egress.

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          Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito.

          O. Billker, V Lindo, M Panico … (1998)
          Malaria is transmitted from vertebrate host to mosquito vector by mature sexual blood-living stages called gametocytes. Within seconds of ingestion into the mosquito bloodmeal, gametocytes undergo gametogenesis. Induction requires the simultaneous exposure to at least two stimuli in vitro: a drop in bloodmeal temperature to 5 degrees C below that of the vertebrate host, and a rise in pH from 7.4 to 8.0-8.2. In vivo the mosquito bloodmeal has a pH of between 7.5 and 7.6. It is thought that in vivo the second inducer is an unknown mosquito-derived gametocyte-activating factor. Here we show that this factor is xanthurenic acid. We also show that low concentrations of xanthurenic acid can act together with pH to induce gametogenesis in vitro. Structurally related compounds are at least ninefold less effective at inducing gametogenesis in vitro. In Drosophila mutants with lesions in the kynurenine pathway of tryptophan metabolism (of which xanthurenic acid is a side product), no alternative active compound was detected in crude insect homogenates. These data could form the basis of the rational development of new methods of interrupting the transmission of malaria using drugs or new refractory mosquito genotypes to block parasite gametogenesis.
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            Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites.

            Paul Gilson, Brendan Crabb (2009)
            The invasion of red blood cells (RBCs) is an essential event in the life cycle of all malaria-causing Plasmodium parasites; however, there are major gaps in our knowledge of this process. Here, we use video microscopy to address the kinetics of RBC invasion in the human malaria parasite Plasmodium falciparum. Under in vitro conditions merozoites generally recognise new target RBCs within 1 min of their release from their host RBC. Parasite entry ensues and is complete on average 27.6s after primary contact. This period can be divided into two distinct phases. The first is an approximately 11s 'pre-invasion' phase that involves an often dramatic RBC deformation and recovery process. The second is the classical 'invasion' phase where the merozoite becomes internalised within the RBC in a approximately 17s period. After invasion, a third 'echinocytosis' phase commences when about 36 s after every successful invasion a dramatic dehydration-type morphology was adopted by the infected RBC. During this phase, the echinocytotic effect reached a peak over the next 23.4s, after which the infected RBC recovered over a 5-11 min period. By then the merozoite had assumed an amoeboid-like state and was apparently free in the cytoplasm. A comparison of our data with that of an earlier study of the distantly related primate parasite Plasmodium knowlesi indicated remarkable similarities, suggesting that the kinetics of invasion are conserved across the Plasmodium genus. This study provides a morphological and kinetic framework onto which the invasion-associated physiological and molecular events can be overlaid.
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              The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage.

              I Weissman, A. Majumdar, K Ikuta … (2000)
              The antigen specificity of a rat monoclonal antibody TER-119 was investigated. In adult mice, TER-119 reacted with mature erythrocytes, 20-25% of bone marrow cells and 2-3% of spleen cells but not with thymocytes nor lymph node cells. In fetal haematopoietic tissues, 30-40% of d 10 yolk sac cells, 80-90% of d 14 fetal liver cells and 40-50% of newborn liver cells were reactive with TER-119. TER-119+ cells in adult bone marrow expressed significant levels of CD45 but not myeloid (Mac-1, Gr-1) or B-cell (B220) markers. Morphological examination and haematopoietic colony-forming assays for isolated TER-119+ cells revealed that TER-119 reacts with erythroid cells at differentiation stages from early proerythroblast to mature erythrocyte, but not with cells showing typical erythroid blast-forming unit (BFU-E) and erythroid colony-forming unit (CFU-E) activities. Erythroleukaemia cell lines do not express the TER-119 antigen even after stimulation with dimethylsulphoxide. TER-119 immunoprecipitated protein bands with molecular masses of 110 kDa, 60 kDa, 52 kDa and 32 kDa from erythrocyte membrane, whereas only a 52-kDa band was detected by TER-119 in Western blot analysis. Further molecular and cellular analyses indicated that the TER-119 antigen is a molecule associated with cell-surface glycophorin A but not with glycophorin A itself.
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                Author and article information

                Contributors
                Inga Siden-Kiamos: inga@imbb.forth.gr
                Journal
                Journal ID (nlm-ta): Sci Rep
                Journal ID (iso-abbrev): Sci Rep
                Title: Scientific Reports
                Publisher: Nature Publishing Group UK (London )
                ISSN (Electronic): 2045-2322
                Publication date (Electronic): 23 February 2018
                Publication date PMC-release: 23 February 2018
                Publication date Collection: 2018
                Volume: 8
                Electronic Location Identifier: 3543
                Affiliations
                [1 ]ISNI 0000 0004 0635 685X, GRID grid.4834.b, Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology - Hellas, ; Heraklion, Greece
                [2 ]ISNI 0000 0004 0576 3437, GRID grid.8127.c, Department of Biology, , University of Crete, ; Heraklion, Greece
                [3 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Bio21 Molecular Science and Biotechnology Institute, Electron Microscopy Unit, , University of Melbourne, Melbourne, ; Victoria, Australia
                [4 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Department of Biochemistry and Molecular Biology, , University of Melbourne, ; Melbourne, Victoria Australia
                [5 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, Université de Montpellier, ; CNRS UMR 5048, INSERM UMR 1054 Montpellier, France
                [6 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, Université de Montpellier, ; CNRS UMR 5235 Montpellier Cedex, France
                [7 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, School of BioSciences, University of Melbourne, Melbourne, ; Victoria, Australia
                Author information
                http://orcid.org/0000-0002-4064-1844
                Article
                Publisher ID: 21801
                DOI: 10.1038/s41598-018-21801-3
                PMC ID: 5824807
                PubMed ID: 29476099
                SO-VID: 0855b161-0df0-44f0-b6e7-ad5d3ea09c3f
                Copyright © © The Author(s) 2018
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                Date received : 5 October 2017
                Date accepted : 2 February 2018
                Categories
                Subject: Article
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                issue-copyright-statement © The Author(s) 2018

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