Band 3 is a host receptor binding merozoite surface protein 1 during thePlasmodium falciparuminvasion of erythrocytes

Abstract

We report the molecular identification of a sialic acid-independent host–parasite interaction in the Plasmodium falciparum malaria parasite invasion of RBCs. Two nonglycosylated exofacial regions of human band 3 in the RBC membrane were identified as a crucial host receptor binding the C-terminal processing products of merozoite surface protein 1 (MSP1). Peptides derived from the receptor region of band 3 inhibited the invasion of RBCs by P. falciparum. A major segment of the band 3 receptor (5ABC) bound to native MSP142 and blocked the interaction of native MSP142 with intact RBCs in vitro. Recombinant MSP119 (the C-terminal domain of MSP142) bound to 5ABC as well as RBCs. The binding of both native MSP142 and recombinant MSP119 was not affected by the neuraminidase treatment of RBCs, but sensitive to chymotrypsin treatment. In addition, recombinant MSP138 showed similar interactions with the band 3 receptor and RBCs, although the interaction was relatively weak. These findings suggest that the chymotrypsin-sensitive MSP1–band 3 interaction plays a role in a sialic acid-independent invasion pathway and reveal the function of MSP1 in the Plasmodium invasion of RBCs

A new release on life: emerging concepts in proteolysis and parasite invasion

“…This is an appealing notion, given the known involvement of EGF-like modules in many protein-protein interactions, but there is little supporting evidence for it. As mentioned above, there are indications that the C-terminal part of MSP1 binds directly or indirectly to host cell receptors at invasion (Goel et al, 2003;Li et al, 2004), but no hint that this requires -or is enhanced by -secondary processing. Furthermore, recent work by Crabb and colleagues showing that the P. falciparum and Plasmodium chabaudi MSP-1 19 domains can be replaced by even highly divergent sequences without any detrimental effect on parasite replication argues for a predominantly structural role for MSP-1 19 (O'Donnell et al, 2000;Drew et al, 2004).…”

“…1B) whereas capping is observed for apical invasion proteins. Shaving occurs continuously as the parasite penetrates and is (Dubremetz et al ., 1985;Grimwood and Smith, 1995) Yes (Mineo and Kasper, 1994;He et al ., 2002) Unknown TgMIC1/MIC4/MIC6 (Meissner et al ., 2002b) Yes (Fourmaux et al ., 1996;Brecht et al ., 2001) MPP1 TgMIC2/M2AP Yes (Carruthers et al ., 1999;Harper et al ., 2004) MPP1 Zhou et al ., 2004) TgMIC3/MIC8 (Meissner et al ., 2002b) Yes (Garcia-Reguet et al ., 2000;Meissner et al ., 2002b) MPP1 TgAMA1 (Donahue et al ., 2000;Hehl et al ., 2000) Unknown MPP1 (S. A. Howell, M. J. Blackman and V. B. Carruthers, unpublished) Plasmodium PfTRAP and PbTRAP (Bhanot et al, 2003;Silvie et al ., 2004) Yes (McCormick et al ., 1999;Akhouri et al ., 2004) Serine protease (Silvie et al .. 2004) PfCSP (Stewart and Vanderberg, 1988; Yes (Pinzon-Ortiz et al ., 2001) Unknown PfMSP1/MSP6/MSP7 (Stafford et al ., 1994) Yes (Goel et al ., 2003;Li et al ., 2004) MESH (Howell et al ., 2003) PkAMA1 and PfAMA1 (Deans et al ., 1984;Howell et al ., 2001) Yes (Fraser et al ., 2001) MESH (Howell et al ., 2003) EBL-DBP (Camus and Hadley, 1985;Haynes et al ., 1988) Yes (Camus and Hadley, 1985;Haynes et al ., 1988) Unknown Py235 (Ogun and Holder, 1996) Yes (Ogun and Holde...…”

“…Nonetheless, at least two possible roles for MSP1 processing can be envisioned. First, as the 42 kDa C-terminal fragment of MSP1 recognizes band 3 on the erythrocyte surface (Goel et al ., 2003), processing could activate MSP1's affinity for this receptor by inducing conformational changes in the adhesive site -analogous to the protease-mediated activation of some viral surface glycoproteins (e.g. Skehel and Wiley, 2000) -or by exposing cryptic binding sites.…”

Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies

“…Initial attachment is thought to involve antigens on the surface of merozoites, such as merozoite surface protein-1 (MSP1) and other GPI-anchored surface proteins (8,9), and is followed by apical reorientation of the merozoite involving apical membrane antigen 1 (AMA1) (10). Secondary interactions are then required for activation of invasion processes.…”

A Key Role for Plasmodium Subtilisin-like SUB1 Protease in Egress of Malaria Parasites from Host Hepatocytes

“…In P. falciparum, PfMSP1 interacts with other MSPs, PfMSP6 and -7, forming a complex on the merozoite surface (46 -48). PfSUB1 matures the three components of this complex (21), which remains associated at the surface of the merozoite and is critical for merozoite invasion, probably via a merozoite-erythrocyte attachment step, prior to parasite reorientation and internalization inside the host cell (23,49,50). More work is needed to unravel the complex basis of merozoite attachment to the erythrocyte and protein maturation events involved in the process.…”