The development of <i>Plasmodium</i> ookinetes <i>in vitro</i>: an ultrastructural study including a description of meiotic division

Sinden, Robert E.; Hartley, R.; Winger, Larry

doi:10.1017/s0031182000057334

Cited by 116 publications

(70 citation statements)

References 27 publications

(35 reference statements)

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“…In this method, Karnovsky's fixative and LXR 112 resin were used to prepare the ookinete cells, which resulted in better structural and organelle integrity and resolution than previously observed in Plasmodium (including the incorrect depiction of rhopties in the apical complex) [17][18][19][20][21][22][23][24][25][26][27][28] and Haemoproteus.…”

Section: Resultsmentioning

confidence: 99%

New Ultrastructural Analysis of the Invasive Apparatus of the Plasmodium Ookinete

Patra¹,

Vinetz²

2012

The American Society of Tropical Medicine and Hygiene

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Abstract. Invasion of the mosquito midgut by the Plasmodium ookinete determines the success of transmission of malaria parasites from humans to mosquitoes and therefore, is a potential target for molecular intervention. Here, we show higher-resolution ultrastructural details of developing and mature P. gallinaceum ookinetes than previously available. Improved fixation and processing methods yielded substantially improved transmission electron micrographs of ookinetes, particularly with regard to visualization of subcellular secretory and other organelles. These new images provide new insights into the synthesis and function of vital invasive machinery focused on the following features: apical membrane protrusions presumptively used for attachment and protein secretion, dark spherical bodies at the apical end of the mature ookinete, and the presence of a dense array of micronemes apposed to microtubules at the apical end of the ookinete involved in constitutive secretion. This work advances understanding of the molecular and cellular details of the Plasmodium ookinete and provides the basis of future, more detailed mechanistic experimentation on the biology of the Plasmodium ookinete.

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Section: Resultsmentioning

confidence: 99%

New Ultrastructural Analysis of the Invasive Apparatus of the Plasmodium Ookinete

Patra¹,

Vinetz²

2012

The American Society of Tropical Medicine and Hygiene

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“…Gene deletion mutants of additional LCCL/LAP protein family members (10,32,33), plasmepsin VI (34) and rhomboid 3 (35), which may be bona fide crystalloid residents, present similar phenotypes with respect to oocyst differentiation. In P. berghei, hemozoin-containing vacuoles accumulate around the crystalloid's edges (4,28). In the DHHC10 knockout, malaria pigment remained scattered throughout the cytoplasm.…”

Section: Discussionmentioning

confidence: 99%

Maternally supplied S-acyl-transferase is required for crystalloid organelle formation and transmission of the malaria parasite

Santos

Duarte

Kehrer

et al. 2016

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

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Transmission of the malaria parasite from the mammalian host to the mosquito vector requires the formation of adequately adapted parasite forms and stage-specific organelles. Here we show that formation of the crystalloid-a unique and short-lived organelle of the Plasmodium ookinete and oocyst stage required for sporogonyis dependent on the precisely timed expression of the S-acyltransferase DHHC10. DHHC10, translationally repressed in female Plasmodium berghei gametocytes, is activated translationally during ookinete formation, where the protein is essential for the formation of the crystalloid, the correct targeting of crystalloid-resident protein LAP2, and malaria parasite transmission.T he malaria parasite is capable of infecting both the vertebrate host and mosquito vector. After a mosquito blood meal, sexual precursor cells rapidly differentiate into mature gametes. In the mosquito midgut, the gametes mate to form a zygote that develops further into the motile ookinete. After crossing the midgut epithelium and establishing a sessile oocyst, the ookinete gives rise to thousands of sporozoites capable of infecting a subsequent mammalian host (1).Sharing key organelles like the nucleus, endoplasmic reticulum, Golgi, and mitochondria with other eukaryotes, this parasite has evolved specialized, stage-specific structures that are necessary for developmental progression during parasite transmission. These include, for example, osmiophilic bodies (secretory vesicles) that release protein factors capable of lysing the parasitophorous vacuole and erythrocyte membranes, thus producing free gametes (2) and a gliding motility motor anchored to the inner membrane complex (IMC), allowing the ookinete to migrate across the mosquito midgut epithelium and establish an oocyst (3). Sporozoite formation in the oocyst finally requires the presence of a stage-specific organelle, the crystalloid, a multivesicular structure assembled in the ookinete and putative reservoir of proteins and lipids used during sporogony. Although this enigmatic organelle was discovered more than 40 y ago, its formation and function remain largely unknown (4-9). Six LCCL proteins have been shown to reside within (9) and maintain the stability (8, 9) of these organelles essential for sporogony (10).The morphological changes taking place during zygote-toookinete development and the generation of thousands of sporozoites inside a single oocyst require extensive protein translation and membrane biogenesis to support the formation of organelles and plasma membrane (PM) surrounding each new parasite. Onethird of the proteins identified in the oocyst and oocyst-derived (midgut) sporozoites of the human parasite Plasmodium falciparum are putatively membrane-bound (11). The targeting of such proteins to organelles, and perhaps formation of certain organelles per se, requires appropriate sorting signals, along with transmembrane (TM) domains to keep these factors in place. Posttranslational modifications, such as lipidation, can increase the affinity of a modif...

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“…The maturation of ookinetes is completed between 19 and 36 h post‐blood meal, and the ookinetes then quickly exit the midgut lumen (Aikawa et al ., 1984; Sinden et al ., 1985; Vlachou et al ., 2004). Ookinete motility appears to be regulated by cGMP levels, because disruption of the gene encoding GCβ in P .…”

Section: The Zygote‐to‐ookinete Conversionmentioning

confidence: 99%

The development of malaria parasites in the mosquito midgut

Bennink

Kiesow

Pradel

2016

Cellular Microbiology

163

155

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SummaryThe mosquito midgut stages of malaria parasites are crucial for establishing an infection in the insect vector and to thus ensure further spread of the pathogen. Parasite development in the midgut starts with the activation of the intraerythrocytic gametocytes immediately after take‐up and ends with traversal of the midgut epithelium by the invasive ookinetes less than 24 h later. During this time period, the plasmodia undergo two processes of stage conversion, from gametocytes to gametes and from zygotes to ookinetes, both accompanied by dramatic morphological changes. Further, gamete formation requires parasite egress from the enveloping erythrocytes, rendering them vulnerable to the aggressive factors of the insect gut, like components of the human blood meal. The mosquito midgut stages of malaria parasites are unprecedented objects to study a variety of cell biological aspects, including signal perception, cell conversion, parasite/host co‐adaptation and immune evasion. This review highlights recent insights into the molecules involved in gametocyte activation and gamete formation as well as in zygote‐to‐ookinete conversion and ookinete midgut exit; it further discusses factors that can harm the extracellular midgut stages as well as the measures of the parasites to protect themselves from any damage.

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The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division

Cited by 116 publications

References 27 publications

New Ultrastructural Analysis of the Invasive Apparatus of the Plasmodium Ookinete

New Ultrastructural Analysis of the Invasive Apparatus of the Plasmodium Ookinete

Maternally supplied S-acyl-transferase is required for crystalloid organelle formation and transmission of the malaria parasite

The development of malaria parasites in the mosquito midgut

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