Plasmodium falciparum: Invasion of Aotus Monkey Red Blood Cells and Adaptation to Aotus Monkeys

Kaneko, O.; Soubes, Sandrine; Miller, Louis H.

doi:10.1006/expr.1999.4441

Cited by 19 publications

(11 citation statements)

References 16 publications

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“…Prewashed normal human erythrocytes and McLeod1 (Kx null ) human erythrocytes were tested for invasion by P. falciparum clones HB3 and D10 as described in ref. 15. The identity of the P. falciparum clones was confirmed by DNA fingerprinting (16).…”

Section: Methodsmentioning

confidence: 94%

Domain III of Plasmodium falciparum apical membrane antigen 1 binds to the erythrocyte membrane protein Kx

Kato

Mayer

Singh

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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Plasmodium falciparum apical membrane antigen 1 (AMA1) is located in the merozoite micronemes, an organelle that contains receptors for invasion, suggesting that AMA1 may play a role in this process. However, direct evidence that P. falciparum AMA1 binds to human erythrocytes is lacking. In this study, we determined that domain III of AMA1 binds to the erythrocyte membrane protein, Kx, and that the rate of invasion of Kx null erythrocytes is reduced, indicating a significant but not unique role of AMA1 and Kx in parasite invasion of erythrocytes. Domains I͞II͞III, domains I͞II and domain III of AMA1 were expressed on the surface of CHO-K1 cells, and their ability to bind erythrocytes was determined. We observed that each of these domains failed to bind untreated human erythrocytes. In contrast, domain III, but not the other domains of AMA1, bound to trypsin-treated human erythrocytes. We tested the binding of AMA1 to trypsin-treated genetically mutant human erythrocytes, missing various erythrocyte membrane proteins. AMA1 failed to bind trypsin-treated Kx null (McLeod) erythrocytes, which lack the Kx protein. Furthermore, treatmentofhumanerythrocyteswithtrypsin,followedby␣-chymotrypsin, cleaved Kx and destroyed the binding of AMA1 to human erythrocytes. Lastly, the rate of invasion of Kx null erythrocytes by P. falciparum was significantly lower than Kx-expressing erythrocytes. Taken together, our data suggest that AMA1 plays an important, but not exclusive, role in invasion of human erythrocytes through a process that involves exposure or modification of the erythrocyte surface protein, Kx, by a trypsin-like enzyme. T he complex multistep process of invasion of erythrocytes byPlasmodium falciparum begins with the binding of any surface of the merozoite, followed by reorientation to put the merozoite's apical end in close apposition to the erythrocyte surface. The apical end of merozoites contains the organelles of invasion, including the micronemes that contain receptors such as members of the Duffy binding protein family of erythrocytebinding ligands (1). A junction forms between P. knowlesi merozoites and the erythrocyte before the merozoite is brought into the erythrocyte. The junction only forms and invasion only occurs between P. knowlesi merozoites and Duffy blood group positive human erythrocytes. Duffy null cells fail to form a junction and are not invaded by P. knowlesi merozoites (2). However, trypsin-or neuraminidase-treated human Duffy null erythrocytes could form a junction and were invaded by P. knowlesi merozoites (3) despite the fact that untreated and trypsin-treated human Duffy null cells fail to bind any of the P. knowlesi Duffy binding proteins expressed on COS-7 cells (2). This result indicates that molecules other than the parasite Duffy binding protein family are exposed by enzyme treatment to form the junction between Duffy negative human erythrocytes and P. knowlesi merozoites. One of the possible junction-forming molecules is apical merozoite antigen 1 (AMA1), which is found in the mic...

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Section: Methodsmentioning

confidence: 94%

Domain III of Plasmodium falciparum apical membrane antigen 1 binds to the erythrocyte membrane protein Kx

Kato

Mayer

Singh

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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“…Invasion Assay-Invasion assays were performed as described previously (32,33). Briefly, 1 ϫ 10 7 target erythrocytes were treated with heparitinase or neuraminidase or incubated with the recombinant protein for 2 h at 37°C.…”

Section: Methodsmentioning

confidence: 99%

“…Briefly, 1 ϫ 10 7 target erythrocytes were treated with heparitinase or neuraminidase or incubated with the recombinant protein for 2 h at 37°C. After they were washed with phosphate-buffered saline, the treated erythrocytes were mixed with 2 ϫ 10 5 iRBC, predominantly early schizont, which were enriched by the Percoll-sorbitol method at 25 h after synchronization with the 5% D-sorbitol method (33). After 20 h, parasitemia of the ring stage parasite was evaluated using Giemsa-stained culture smears.…”

Section: Methodsmentioning

confidence: 99%

Plasmodium falciparum BAEBL Binds to Heparan Sulfate Proteoglycans on the Human Erythrocyte Surface

Kobayashi

Kato

Sugi

et al. 2010

Journal of Biological Chemistry

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Erythrocyte invasion is critical to the pathogenesis and survival of the malarial parasite, Plasmodium falciparum. This process is partly mediated by proteins that belong to the Duffy binding-like family, which are expressed on the merozoite surface. One of these proteins, BAEBL (also known as EBA-140), is thought to bind to glycophorin C in a sialic acid-dependent manner. In this report, by the binding assay between recombinant BAEBL protein and enzyme-treated erythrocytes, we show that the binding of BAEBL to erythrocytes is mediated primarily by sialic acid and partially through heparan sulfate (HS). Because BAEBL binds to several kinds of HS proteoglycans or purified HS, the BAEBL-HS binding was found to be independent of the HS proteoglycan peptide backbone and the presence of sialic acid moieties. Furthermore, both the sialic acid-and HS-dependent binding were disrupted by the addition of soluble heparin. This inhibition may be the result of binding between BAEBL and heparin. Invasion assays demonstrated that HS-dependent binding was related to the efficiency of merozoite invasion. These results suggest that HS functions as a factor that promotes the binding of BAEBL and merozoite invasion. Moreover, these findings may explain the invasion inhibition mechanisms observed following the addition of heparin and other sulfated glycoconjugates.Malaria caused by Plasmodium falciparum kills approximately 1 million people per year. After entering the human bloodstream, the parasite propagates asexually via repeated cycles of erythrocyte invasion, cell division, and cell rupture. The process by which the parasitic merozoites invade erythrocytes involves the following steps: attachment, apical reorientation, junction formation, and the formation of a protective parasitophorous vacuole (1).The Duffy binding-like (DBL) 2 family is composed of adhesion molecules that are critical for junction formation between the apical end of the merozoite and the erythrocyte surface.Proteins in this family, such as EBA-175 (erythrocyte-binding antigen-175), are homologous to Plasmodium vivax Duffybinding protein. These proteins contain one or more DBL domains, which are composed of conserved cysteine residues and are associated with erythrocyte binding (2). EBA-175 is bound to glycophorin A on the erythrocyte surface in a sialic acid-dependent manner (3). However, erythrocytes that are treated with neuraminidase remain susceptible to the merozoites of some clones (4), indicating the existence of sialic acidindependent invasion pathways. These alternative pathways are thought to be mediated, at least in part, by other members of the DBL family (5).Parasite growth is inhibited by the addition of heparin, some sulfated saccharide anions, and sulfated chemical compounds (6 -11). Although the inhibition mechanisms remain unclear, these reports suggest the possibility that sulfated moieties play a role in merozoite invasion. In addition to invasion, heparan sulfate (HS) is believed to function as a receptor for PfEMP1 (P. falciparum erythr...

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“…The parasite lines examined originated from Southeast Asia (Dd2, FVO, Camp, T9/96, T9/102, K1, and Thai838), Papua New Guinea (MAD20), Central and South America (HB3, 7G8, DIV17, DIV29, DIV30, PC49, PC54, Santa Lucia, and Haiti), and Africa (RO33, 123/5, 128/4, SL/D6, LF4/1, 102/1, M2, M5, Fab9, 713, P13, and KMWII) and have been previously described [23][24][25]. Their geographic origins have also been previously described [26].…”

Section: Malaria Parasitesmentioning

confidence: 96%

“…Genomic DNA was obtained as described previously [24]. Total RNA was isolated from schizont stage-enriched HB3 and Dd2 parasite lines using the RNeasy mini kit (Qiagen, Valencia, CA).…”

Section: Dna and Rna Isolationmentioning

confidence: 99%

Diversity and evolution of the rhoph1/clag multigene family of Plasmodium falciparum

Iriko

Kaneko

Otsuki

et al. 2008

Molecular and Biochemical Parasitology

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A complex of high molecular mass proteins (PfRhopH) of the human malaria parasite Plasmodium falciparum induces host protective immunity and therefore is a candidate for vaccine development. Understanding the level of polymorphism and the evolutionary processes is important for advancements in both vaccine design and knowledge of the evolution of cell invasion in this parasite. In the present study, we sequenced the entire open reading frames of seven genes encoding the proteins of the PfRhopH complex (rhoph2, rhoph3, and five rhoph1/clag gene paralogs). We found that four rhoph1/clag genes (clag2, 3.1, 3.2, and 8) were highly polymorphic. Amino acid substitutions and indels are predominantly clustered around amino acid positions 1000-1200 of these four rhoph1/clag genes. An excess of nonsynonymous substitutions over synonymous substitutions was detected for clag8 and 9, indicating positive selection. The McDonald-Kreitman test with a Plasmodium reichenowi orthologous sequence also supports positive selection on clag8. Based on the ratio of interspecific genetic distance to intraspecific distance, the time to the most recent common ancestor of the clag2 and 8 polymorphisms was estimated to be 1.89 and 0.87 million years ago, respectively, assuming divergence of P. falciparum and P. reichenowi 6 million years ago. In addition to a copy number polymorphism, gene conversion events were detected for the rhoph1/clag genes on chromosome 3, which likely play a role in increasing the diversity of each locus. Our results indicate that a high diversity of the PfRhopH1/Clag multigene family is maintained by diversifying selection forces over a considerably long period.

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Plasmodium falciparum: Invasion of Aotus Monkey Red Blood Cells and Adaptation to Aotus Monkeys

Cited by 19 publications

References 16 publications

Domain III of Plasmodium falciparum apical membrane antigen 1 binds to the erythrocyte membrane protein Kx

Domain III of Plasmodium falciparum apical membrane antigen 1 binds to the erythrocyte membrane protein Kx

Plasmodium falciparum BAEBL Binds to Heparan Sulfate Proteoglycans on the Human Erythrocyte Surface

Diversity and evolution of the rhoph1/clag multigene family of Plasmodium falciparum

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