Sporogonic Development of Plasmodium yoelii in Five Anopheline Species

Vaughan, Jefferson A.; Hensley, Lisa E.; Beier, John C.

doi:10.2307/3283245

Cited by 67 publications

(43 citation statements)

References 19 publications

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“…Oocysts developing beneath the midgut basal lamina are thought to be in a privileged site and protected from the hemolymph antimicrobial peptides by a capsule composed, in part, of components of the basal lamina (1). Unlike the midgut and sporozoite stages, little parasite death occurs naturally at this stage (37,38). Our findings suggest that the small peptide Vida3 can gain access to the developing oocyst via the hemocoel.…”

Section: Discussionmentioning

confidence: 76%

Design and Activity of Antimicrobial Peptides against Sporogonic-Stage Parasites Causing Murine Malarias

Arrighi

Nakamura

Miyake

et al. 2002

Antimicrob Agents Chemother

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Insects produce several types of peptides to combat a broad spectrum of invasive pathogenic microbes, including protozoans. However, despite this defense response, infections are often established. Our aim was to design novel peptides that produce high rates of mortality among protozoa of the genus Plasmodium, the malaria parasites. Using existing antimicrobial peptide sequences as templates, we designed and synthesized three short novel hybrids, designated Vida1 to Vida3. Each has a slightly different predicted secondary structure. The peptides were tested against sporogonic stages of the rodent malaria parasites Plasmodium berghei (in vitro and in vivo) and P. yoelii nigeriensis (in vitro). The level of activity varied for each peptide and according to the parasite stage targeted. Vida3 (which is predicted to have large numbers of ␤ sheets and coils but no ␣ helices) showed the highest level of activity, killing the early sporogonic stages in culture and causing highly significant reductions in the prevalence and intensity of infection of P. berghei after oral administration or injection in Anopheles gambiae mosquitoes. The secondary structures of these peptides may play a crucial role in their ability to interact with and kill sporogonic forms of the malaria parasite.

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Section: Discussionmentioning

confidence: 76%

Design and Activity of Antimicrobial Peptides against Sporogonic-Stage Parasites Causing Murine Malarias

Arrighi

Nakamura

Miyake

et al. 2002

Antimicrob Agents Chemother

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“…Sporozoites that fail to reach and penetrate the salivary glands are quickly cleared by the mosquito immune system (22). Previous studies with trap(Ϫ) and maebl(Ϫ) parasites showed that a block in life cycle progression translates into accumulation of hemocoel sporozoites.…”

Section: Discussionmentioning

confidence: 99%

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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“…The finding of midgut-based TBI in both human and rodent malaria models is noteworthy because different Plasmodium species display different developmental kinetics in the mosquito (12)(13)(14)(15)(16).…”

Section: Discussionmentioning

confidence: 99%

Anti-mosquito midgut antibodies block development of Plasmodium falciparum and Plasmodium vivax in multiple species of Anopheles mosquitoes and reduce vector fecundity and survivorship

Lal

Patterson

Sacci

et al. 2001

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

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The mosquito midgut plays a central role in the sporogonic development of malaria parasites. We have found that polyclonal sera, produced against mosquito midguts, blocked the passage of Plasmodium falciparum ookinetes across the midgut, leading to a significant reduction of infections in mosquitoes. Anti-midgut mAbs were produced that display broad-spectrum activity, blocking parasite development of both P. falciparum and Plasmodium vivax parasites in five different species of mosquitoes. In addition to their parasite transmission-blocking activity, these mAbs also reduced mosquito survivorship and fecundity. These results reveal that mosquito midgut-based antibodies have the potential to reduce malaria transmission in a synergistic manner by lowering both vector competence, through transmission-blocking effects on parasite development, and vector abundance, by decreasing mosquito survivorship and egg laying capacity. Because the intervention can block transmission of different malaria parasite species in various species of mosquitoes, vaccines against such midgut receptors may block malaria transmission worldwide.O f the several hundred species of Anopheles mosquitoes worldwide, only about 20 are major vectors of human malaria. Several components contribute to this fact, including the propensity of a given species to feed on humans, the average longevity of a mosquito species, and the innate ability of a species to permit development of the parasite (i.e., vector competence). Different intervention strategies attempt to reduce malaria transmission by reducing these various components. Reducing vector competence is the primary objective behind two rapidly evolving areas of research in malaria and other vector-borne diseases, namely the replacement of natural vector populations with populations genetically engineered for refractoriness and transmission-blocking immunity (TBI).Transmission-blocking vaccines in malaria are envisioned to inhibit the developmental stages of the malaria parasites in the mosquito midgut. The first 48 h after ingestion of an infective blood meal is the most critical time period for malaria parasite development within the mosquito. It is during this time that the parasite fertilization takes place and the resulting zygotes transform into motile ookinetes. Ookinetes traverse the midgut and lodge between the basal lamina and midgut epithelia, where they encyst and develop into sporozoite-producing oocysts.Several studies with rodent and human malaria parasites have revealed that the ookinete-to-oocyst transition is the most vulnerable link in sporogonic development of malaria parasites (1-3). Thus, the developing parasite stages in the mosquito midgut provide an ideal target for transmission-blocking vaccines. Efforts in transmission-blocking vaccines in malaria have focused primarily on the use of specific parasite antigens as targets of immune intervention in the mosquito midgut. Antibodies against parasite antigens block fertilization and͞or prevent the movement of ookinetes across the...

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Sporogonic Development of Plasmodium yoelii in Five Anopheline Species

Cited by 67 publications

References 19 publications

Design and Activity of Antimicrobial Peptides against Sporogonic-Stage Parasites Causing Murine Malarias

Design and Activity of Antimicrobial Peptides against Sporogonic-Stage Parasites Causing Murine Malarias

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

Anti-mosquito midgut antibodies block development of Plasmodium falciparum and Plasmodium vivax in multiple species of Anopheles mosquitoes and reduce vector fecundity and survivorship

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