The microneme proteins CTRP and SOAP are not essential for Plasmodium berghei ookinete to oocyst transformation in vitro in a cell free system

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Abstract

Background

Two Plasmodium berghei ookinete micronemal proteins, circumsporozoite and TRAP related protein (CTRP) and secreted ookinete adhesive protein (SOAP) both interact with the basal lamina component laminin. Following gene disruption studies it has been proposed that, apart from their role in motility, these proteins may be required for interactions leading to ookinete-to-oocyst transformation.

Methods

CTRP and SOAP null mutant P. berghei ookinetes were compared to P. berghei ANKA wild-type for their ability to transform and grow in vitro. To confirm in vitro findings for P. berghei CTRP-KO ookinetes were injected into the haemocoel of Anopheles gambiae female mosquitoes.

Results

Transformation, growth, and viability were comparable for the gene disrupted and wild-type parasites. P. berghei CTRP-KO ookinetes were able to transform into oocysts in the haemocoel of An. gambiae mosquitoes.

Conclusion

Neither CTRP nor SOAP is required for parasite transformation in vitro. By-passing the midgut lumen allows for the transformation of P. berghei CTRP-KO ookinetes suggesting that it is not required for transformation in vivo.

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Most cited references 41

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CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts.

Yasuo Chinzei, Tohru Kariu, Kazuhiko Yano … (2006)

The malarial parasite has two hosts in its life cycle, a vertebrate and a mosquito. We report here that malarial invasion into these hosts is mediated by a protein, designated cell-traversal protein for ookinetes and sporozoites (CelTOS), which is localized to micronemes that are organelles for parasite invasive motility. Targeted disruption of the CelTOS gene in Plasmodium berghei reduced parasite infectivity in the mosquito host approximately 200-fold. The disruption also reduced the sporozoite infectivity in the liver and almost abolished its cell-passage ability. Liver infectivity was restored in Kupffer cell-depleted rats, indicating that CelTOS is necessary for sporozoite passage from the circulatory system to hepatocytes through the liver sinusoidal cell layer. Electron microscopic analysis revealed that celtos-disrupted ookinetes invade the midgut epithelial cell by rupturing the cell membrane, but then fail to cross the cell, indicating that CelTOS is necessary for migration through the cytoplasm. These results suggest that conserved cell-passage mechanisms are used by both sporozoites and ookinetes to breach host cellular barriers. Elucidation of these mechanisms might lead to novel antimalarial strategies to block parasite's transmission.

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CTRP is essential for mosquito infection by malaria ookinetes.

J T Dessens, A Beetsma, G Dimopoulos … (1999)

The malaria parasite suffers severe population losses as it passes through its mosquito vector. Contributing factors are the essential but highly constrained developmental transitions that the parasite undergoes in the mosquito midgut, combined with the invasion of the midgut epithelium by the malaria ookinete (recently described as a principal elicitor of the innate immune response in the Plasmodium-infected insect). Little is known about the molecular organization of these midgut-stage parasites and their critical interactions with the blood meal and the mosquito vector. Elucidation of these molecules and interactions will open up new avenues for chemotherapeutic and immunological attack of parasite development. Here, using the rodent malaria parasite Plasmodium berghei, we identify and characterize the first microneme protein of the ookinete: circumsporozoite- and TRAP-related protein (CTRP). We show that transgenic parasites in which the CTRP gene is disrupted form ookinetes that have reduced motility, fail to invade the midgut epithelium, do not trigger the mosquito immune response, and do not develop further into oocysts. Thus, CTRP is the first molecule shown to be essential for ookinete infectivity and, consequently, mosquito transmission of malaria.

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P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions.

Bronwyn G. Butcher, C Janse, A Beetsma … (2001)

The ookinete surface proteins (P25 and P28) are proven antimalarial transmission-blocking vaccine targets, yet their biological functions are unknown. By using single (Sko) and double gene knock-out (Dko) Plasmodium berghei parasites, we show that P25 and P28 share multiple functions during ookinete/oocyst development. In the midgut of mosquitoes, the formation of ookinetes lacking both proteins (Dko parasites) is significantly inhibited due to decreased protection against lethal factors, including protease attack. In addition, Dko ookinetes have a much reduced capacity to traverse the midgut epithelium and to transform into the oocyst stage. P25 and P28 are partially redundant in these functions, since the efficiency of ookinete/oocyst development is only mildly compromised in parasites lacking either P25 or P28 (Sko parasites) compared with that of Dko parasites. The fact that Sko parasites are efficiently transmitted by the mosquito is a compelling reason for including both target antigens in transmission-blocking vaccines.

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Author and article information

Journal

Journal ID (nlm-ta): Malar J

Title: Malaria Journal

Publisher: BioMed Central

ISSN (Electronic): 1475-2875

Publication date Collection: 2008

Publication date (Electronic): 19 May 2008

Volume: 7

Page: 82

Affiliations

[1 ]Centre for Applied Entomology and Parasitology, Institute of Science and Technology in Medicine, School of Life Sciences, Keele University, Staffordshire, ST5 5BG, UK

Article

Publisher ID: 1475-2875-7-82

DOI: 10.1186/1475-2875-7-82

PMC ID: 2427035

PubMed ID: 18489758

SO-VID: 7d5ba609-9d66-4c29-a042-5fc9e98ad5e6

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The microneme proteins CTRP and SOAP are not essential for Plasmodium berghei ookinete to oocyst transformation in vitro in a cell free system

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Herbal Medicines Journal (Herb Med J)

Most cited references 41

CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts.

CTRP is essential for mosquito infection by malaria ookinetes.

P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions.

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