Getting infectious: formation and maturation of Plasmodium sporozoites in the Anopheles vector

Matuschewski, Kai

doi:10.1111/j.1462-5822.2006.00778.x

Cited by 66 publications

(54 citation statements)

References 80 publications

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“…Because this is the only growth and replication phase in the Plasmodium life cycle that occurs outside, yet closely associated with, host cells (2,4), it is conceivable that infectious and immunogenic sporozoites might be produced without the need for a mosquito vector. In a landmark study, Alon Warburg and Louis Miller seeded purified P. gallinaceum ookinetes onto Matrigel and Drosophila melanogaster L2 feeder cells and obtained spherical and elongated oocysts (41).…”

Section: Discussionmentioning

confidence: 99%

“…Sporozoites are passively transported by the slow hemolymph circulation and will eventually pass the basal lamina of salivary glands. Here, sporozoites attach, penetrate the acinar cells, and accumulate in the salivary duct, marking the final step of sporogony (3,4). During this passage, sporozoites mature and acquire traits that are essential to colonize a new vertebrate host.…”

mentioning

confidence: 99%

“…When an infectious female Anopheles mosquito probes for a blood vessel, she injects most sporozoites intradermally. Salivary gland sporozoites accomplish continuous and fast gliding locomotion, transmigration of cellular barriers, invasion of hepatocytes, and formation of a replicationcompetent niche, the parasitophorous vacuole (4). In marked contrast, young midgut-associated sporozoites lack these abilities (5).…”

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confidence: 99%

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Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

2014

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bMalaria is a vector-borne disease caused by the single-cell eukaryote Plasmodium. The infectious parasite forms are sporozoites, which originate from midgut-associated oocysts, where they eventually egress and reach the mosquito hemocoel. Sporozoites actively colonize the salivary glands in order to be transmitted to the mammalian host. Whether residence in the salivary glands provides distinct and vital cues for the development of infectivity remains unsolved. In this study, we systematically compared the infectivity of Plasmodium berghei sporozoites isolated from the mosquito hemocoel and salivary glands. Hemocoel sporozoites display a lower proportion of gliding motility but develop into liver stages when added to cultured hepatoma cells or after intravenous injection into mice. Mice infected by hemocoel sporozoites had blood infections similar to those induced by sporozoites liberated from salivary glands. These infected mice display indistinguishable systemic inflammatory cytokine responses and develop experimental cerebral malaria. When used as metabolically active, live attenuated vaccine, hemocoel sporozoites elicit substantial protection against sporozoite challenge infections. Collectively, these findings show that salivary gland colonization does not influence parasite virulence in the mammalian host when sporozoites are administered intravenously. This conclusion has important implications for in vitro sporozoite production and manufacturing of whole-sporozoite vaccines.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

2014

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“…Among these, mosquitoes (Culicidae) are the most epidemiologically significant pests and disease vectors, as they transmit deadly human and animal pathogens such as the causative agents of malaria, lymphatic filariasis and dengue hemorrhagic fever. During their natural life cycle, these pathogens are ingested with infective blood meals, cross the midgut epithelium, and enter the hemocoel, where they migrate to the salivary glands or mouthparts (Hillyer et al, 2007;Matuschewski, 2006;Salazar et al, 2007). Understanding the physiological basis of hemolymph flow may increase our knowledge on how these parasites undergo this obligate migration.…”

Section: Introductionmentioning

confidence: 99%

Structural mechanics of the mosquito heart and its function in bidirectional hemolymph transport

Glenn

King

Hillyer

2010

Journal of Experimental Biology

187

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SUMMARYThe insect circulatory system transports nutrients, signaling molecules, wastes and immune factors to all areas of the body. The primary organ driving circulation is the dorsal vessel, which consists of an abdominal heart and a thoracic aorta. Here, we present qualitative and quantitative data characterizing the heart of the mosquito, Anopheles gambiae. Visual observation showed that the heart of resting mosquitoes contracts at a rate of 1.37Hz (82 beats per minute) and switches contraction direction, with 72% of contractions occurring in the anterograde direction (toward the head) and 28% of contractions occurring in the retrograde direction (toward the tip of the abdomen). The heart is tethered to the midline of the abdominal tergum by six complete and three incomplete pairs of alary muscles, and propels hemolymph at an average velocity of 8mms -1 by sequentially contracting muscle fibers oriented in a helical twist with respect to the lumen of the vessel. Hemolymph enters the heart through six pairs of incurrent abdominal ostia and one pair of ostia located at the thoraco-abdominal junction that receive hemolymph from the abdominal hemocoel and thoracic venous channels, respectively. The vessel expels hemolymph through distal excurrent openings located at the anterior end of the aorta and the posterior end of the heart. In conclusion, this study presents a comprehensive revision and expansion of our knowledge of the mosquito heart and for the first time quantifies hemolymph flow in an insect while observing dorsal vessel contractions. Supplementary material available online at

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“…Colonization of the salivary glands by Plasmodium parasites is driven by a number of stage-specific surface proteins (9), including (i) the major sporozoite surface protein circumsporozoite protein (CSP) (18), (ii) the sporozoite adhesin apical membrane antigen/erythrocyte binding-like protein (MAEBL) (8), and (iii) the sporozoite invasin thrombospondin-related anonymous protein (TRAP) (7,10,17,24). However, none of these proteins are conserved across apicomplexan hemoprotozoa, indicating a high degree of parasite/invertebrate host coadaptation.…”

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Disruption of Plasmodium Sporozoite Transmission by Depletion of Sporozoite Invasion-Associated Protein 1

2009

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Accumulation of infectious Plasmodium sporozoites in Anopheles spp. salivary glands marks the final step of the complex development of the malaria parasite in the insect vector. Sporozoites are formed inside midgutassociated oocysts and actively egress into the mosquito hemocoel. Traversal of the salivary gland acinar cells correlates with the sporozoite's capacity to perform continuous gliding motility. Here, we characterized the cellular role of the Plasmodium berghei sporozoite invasion-associated protein 1 (SIAP-1). Intriguingly, SIAP-1 orthologs are found exclusively in apicomplexan hemoprotozoa, parasites that are transmitted by arthropod vectors, e.g., Plasmodium, Babesia, and Theileria species. By fluorescent tagging with mCherry, we show that SIAP-1 is expressed in oocyst-derived and salivary gland-associated sporozoites, where it accumulates at the apical tip. Targeted disruption of SIAP-1 does not affect sporozoite formation but causes a partial defect in sporozoite egress from oocysts and abolishes sporozoite colonization of mosquito salivary glands. Parasites with the siap-1(؊) mutation are blocked in their capacity to perform continuous gliding motility. We propose that arthropod-transmitted apicomplexan parasites specifically express secretory factors, such as SIAP-1, that mediate efficient oocyst exit and migration to the salivary glands.Protozoan parasites of the phylum Apicomplexa have adopted an obligate intracellular life-style in a wide range of animal hosts. Apicomplexan parasites share many characteristics, including a set of apical specialized secretory organelles, active substrate-dependent locomotion, and compartmentalization of biosynthetic pathways in apicoplasts. Transmission to the vertebrate hosts occurs via tailor-made motile parasite stages, termed sporozoites, which are formed inside oocysts, the only extracellular replication phase during the complex apicomplexan life cycles. However, apicomplexan parasites differ fundamentally in their transmission modes. Coccidian parasites, such as Toxoplasma gondii, the causative agent of toxoplasmosis, and cryptosporidia, which can cause life-threatening diarrhea, form oocysts that are taken up orally via contaminated food or water, respectively. After accidental ingestion, sporozoites are liberated from the oocysts and breach or directly invade the intestinal endothelium to commence an infection. In marked contrast, sporozoites of apicomplexan hemoprotozoa are inoculated intradermally by arthropod vectors, e.g., Anopheles mosquitoes or ticks. Sporozoites then actively leave the inoculation site and enter the blood circulation (3). In the case of Plasmodium species, the causative agents of malaria, sporozoites are formed in midgut-associated oocysts (16), actively exit the oocyst (1, 23), and penetrate the distal portion of the lateral salivary gland lobes where they eventually accumulate, rendering the infected mosquito infectious to the vertebrate host (4).Colonization of the salivary glands by Plasmodium parasites is driven by a number ...

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Getting infectious: formation and maturation of Plasmodium sporozoites in the Anopheles vector

Cited by 66 publications

References 80 publications

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

Plasmodium berghei Sporozoites Acquire Virulence and Immunogenicity during Mosquito Hemocoel Transit

Structural mechanics of the mosquito heart and its function in bidirectional hemolymph transport

Disruption of Plasmodium Sporozoite Transmission by Depletion of Sporozoite Invasion-Associated Protein 1

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