Chapter 9 : The Sporozoite

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The intense interest in sporozoite biology has been richly rewarded by the progressive unravelling of the truly remarkable journey undertaken by such a simple cell. The diversity and elegance of the strategies employed are only now being revealed. The key new comprehensive technologies underpinning these advances in our understanding includes ; ; ; . The sporozoite is one of three invasive stages in the malaria life cycle. The others are the ookinete and the merozoite. Sporozoite formation is the final step of differentiation of the oocyst. Sporozoite-infected epithelial cells can be expelled from the midgut wall into the lumen of the gut in a manner highly reminiscent of the time bomb theory of ookinete-midgut interaction. The salivary glands present a significant barrier to sporozoite development. Only sporozoites isolated from salivary glands confer significant sterile protection. Sporozoite maturation correlates with a dramatic increase of gliding motility, a unique form of substrate-dependent locomotion, and infectivity to the mammalian host. Sporozoites glide extensively through the avascular dermis until they reach a capillary. Having penetrated through the basal side of the endothelial cell layer, a proportion of sporozoites invade blood vessels and get carried away by the blood flow, whereas others actively enter lymph vessels or remain as residual sporozoites in the skin tissue. The recognition of the final target cell would then switch the parasite’s program from transmigration to productive entry by simultaneous formation of a parasitophorous vacuole.

Citation: Sinden R, Matuschewski K. 2005. The Sporozoite, p 169-190. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch9

Key Concept Ranking

Malaria Life Cycle
Microtubule Organizing Centers
Nitric Oxide Synthase
Spindle Pole Bodies
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Image of FIGURE 1

Diagram illustrating the morphogenesis of one sporozoite on the surface of the sporoblast in the malarial oocyst. Initial bud formation (P. berghei day 7 to 8) (A); intermediate elongation (day 9 to 10) (B); elongate but immature sporozoite (day 11) (C).N, nucleus;A, apicoplast; Mit, mitochondrion; Rh, rhoptry (a regulated secretory vesicle); M, microneme (a regulated secretory vesicle); SPB, spindle pole body; er, endoplasmic reticulum.

Citation: Sinden R, Matuschewski K. 2005. The Sporozoite, p 169-190. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch9
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Image of FIGURE 2

Diagram illustrating some of the separate cellular activities that make up the cell cycle of the malarial oocyst (based on a model proposed for ).The time scale is indicated at the bottom of the diagram, and the possible times at which different gene knockouts exert their impact on development are shown at the top.The diagram attempts to illustrate the difficulty in correctly assigning a point of biological impact of any gene knockout. If morphological criteria alone are used, it will depend in which subcycle the mutant acts as to when the aberrant phenotype is seen. Also noting the interdependence of the subcycles, it is perfectly feasible to ascribe a late phenotype to a mutant with an early action but with a morphological phenotype visible only following its interaction with a second and previously unaffected subcycle, for example.

Citation: Sinden R, Matuschewski K. 2005. The Sporozoite, p 169-190. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch9
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Image of FIGURE 3

Role of the sporozoite molecular motor during host cell invasion. Sporozoites actively invade their respective host cells under simultaneous formation of a novel cellular compartment of the host cell’s own making, the parasitophorous vacuole (PV). The PV membrane is remodeled through the secretion of proteins and lipids from secretory organelles, i.e., micronemes (Mn), rhoptries (Rh), and dense granules.The sporozoite invasin TRAP interacts with as-yet-unidentified cellular receptors leading to formation of a tight moving junction. This junction acts as a molecular sieve to exclude host plasma membrane proteins.Through its conserved cytoplasmic domain,TRAP is tethered via aldolase tetramers to short actin filaments. Actin polymerization is temporarily and spatially regulated and is likely to be the rate-limiting factor for parasite locomotion. Unconventional class XIV myosins (MyoA) are immobilized via myosin A tail domain interacting protein (MTIP) and other proteins to the IMC,flattened membrane stacks that are anchored to subpellicular filaments and microtubules. This structure determines the shape of sporozoites and serves as the scaffold for actin-myosin-based motility. Plus-end-directed motility along the actin units results in backward translocation of the actin oligomers to the posterior end of the parasite and, thus, a net forward movement of the sporozoite.

Citation: Sinden R, Matuschewski K. 2005. The Sporozoite, p 169-190. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch9
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Generic image for table

Characteristics of some proteins expressed in sporozoites

Note that the table is a nonexhaustive list of sporozoite proteins. Predicted molecular weights are shown in brackets and may vary between and other species. Predicted primary structures are not to scale; stripes indicate repeat regions, grey and black boxes indicate putative cleavable signal peptides and transmembrane spans, respectively. Cellular location is typically assigned by fluorescence microscopy and stage specificity by Western and/or reverse transcription-PCR. Putative function is based on reverse genetic data (italics) or recombinant protein expression and/or antibody inhibition studies (Roman). References are listed for sporozoite expression studies only.Abbreviations: I to III,AMA-1 domains; 6-Cys, six-cysteine motif;A-domain, von Willebrand factor A domain;AMA- 1, apical membrane antigen 1;ATSR, altered thrombospondin repeat;CSP, circumsporozoite protein;CTD,TRAP family cytoplasmic tail domain; Cys, cysteine-rich domain; GPI, gycosylphospatidylinositol anchor; IMC1a, inner membrane complex protein 1a;LCAT, lecithincholesterol acyltransferase;LCCL, factor C; Coch-5b2, Lgl1 domain; LH2, lipoxygenase domain; M1 and M2, MAEBL ligand domains; MACPF, membrane attack complex/perforin; MAEBL, apical membrane antigen/erythrocyte binding-like protein; MCP1, merozoite- capping protein 1; P52, six-cysteine family protein of 52 kDa; PL, phospholipase; PLP1, perforin-like protein 1; PR, peroxiredoxin; PTX, pentraxin domain; RI, region I; RIII, region III; SPATR, secreted protein with altered thrombospondin repeat; SPECT, sporozoite microneme protein essential for cell traversal; SR, scavenger receptor-like protein; SRCR, scavenger receptor cysteine rich; STARP, sporozoite threonine and asparagine-rich protein;TRAP, thrombospondin-related anonymous protein;TSR, thrombospondin type I repeat; UIS3 and UIS4, upregulated in infective sporozoites proteins 3 and 4.

Citation: Sinden R, Matuschewski K. 2005. The Sporozoite, p 169-190. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch9

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