Molecular mechanisms of host cell traversal by malaria sporozoites

Yang, Annie S. P.; Boddey, Justin A

doi:10.1016/j.ijpara.2016.09.002

Cited by 18 publications

(11 citation statements)

References 67 publications

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“…Transgenic lines were able to egress after both the 165 control DMSO treatment and upon rapamycin induced gene excision, but the 166 merozoite-hemozoin distance was significantly reduced in the latter case ( Figure 167 3C). When apical membrane antigen 1 (AMA1), a microneme protein important for 168 erythrocyte attachment during invasion but unlikely to be involved in merozoite 169 motility (Treeck, et al, 2009;Yang et al, 2017), was conditionally deleted, parasites 170 were able to efficiently egress and motility assayed by the merozoite-hemozoin 171 distance was not affected ( Figure S3). These results confirm the involvement of the 172 glideosome in Plasmodium merozoite gliding motility.…”

Section: Gliding Motility Is Powered By An Actomyosin Motor and Glidementioning

confidence: 99%

Gliding motility of Plasmodium merozoites

Yahata

Hart

Davies

et al. 2020

Preprint

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18Plasmodium malaria parasites use a unique form of locomotion termed gliding 19 motility to move through host tissues and invade cells. The process is substrate-20 dependent and powered by an actomyosin motor that drives the posterior 21 translocation of extracellular adhesins, which in turn propel the parasite forward. 22Gliding motility is essential for tissue translocation in the sporozoite and ookinete 23 stages, however, the short-lived erythrocyte-invading merozoite stage has never 24 been observed to undergo gliding movement. Here for the first time we reveal that 25 blood stage Plasmodium merozoites use gliding motility for translocation in addition 33 Keywords 34Malaria, Merozoite, Erythrocyte invasion, Gliding motility 35 36 (Russell et al., 1981; Dobrowolski et al., 1996). The system instead relies on the 41 apical presentation of parasite transmembrane adhesins which bind to host 42 substrates and then are drawn towards the parasite posterior by a conserved 43 actomyosin motor running under the surface of the plasma membrane, resulting in 44 the forward propulsion of the parasite (Tardieux et al., 2016; Frenal et al., 2017). 45Motility of invasive forms of malarial parasites (termed "zoites") was first described 46 for the ookinete stage in avian blood (Danilewsky et al., 1889), and then for the 47 sporozoite stage in the mosquito (Grassi et al., 1900). Unlike ookinetes and 48 sporozoites, which must traverse through tissues, no gliding motility has been 49 described for the merozoite, which invades erythrocytes in the bloodstream. Instead, 50 only limited reorientation movement and cellular deformation has been observed 51 across several malarial parasite species, including Plasmodium knowlesi, P. 52 falciparum, and P. yoelii (Dvorak et al., 1975; Gilson et al., 2009;Yahata et al., 2012). 53Due to the short-lived nature and diminished size of merozoites (1-2 µm) relative to 54 other zoites, it was presumed that merozoites do not require motility to encounter 55 erythrocytes in the bloodstream, leading to the consensus that the molecular motor 56 is principally required for penetration of the erythrocyte during invasion (Tardieux et 57 al., 2016). 58Here we show that both P. falciparum and P. knowlesi are capable of gliding 59 motility across both erythrocyte surfaces and polymer coverslips, with distinctive 60 dynamics between the two species. We have additionally developed a scalable 61 65 Results 66 Gliding motility of Plasmodium merozoites 67Here we sought to address the long-standing question of whether malarial 68 merozoites undergo conventional gliding motility. Whilst motility of sporozoites is 69 normally observed on bovine serum albumin-coated glass slides, merozoites do not 70 glide on this substrate. However, when using polymer coverslips with a hydrophilic 71 coating (ibiTreat), we observed motile merozoites. When imaged immediately after 72 erythrocyte egress, merozoites show directional movement on the coverslip surface 73 which displaces them from the hemozoin containing residual b...

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Section: Gliding Motility Is Powered By An Actomyosin Motor and Glidementioning

confidence: 99%

Gliding motility of Plasmodium merozoites

Yahata

Hart

Davies

et al. 2020

Preprint

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“…Previous work reported that Pf PLP1 was expressed in blood stages and mediates the calcium-dependent egress of merozoites from erythrocytes [ 39 ]. However, studies with P. falciparum parasites expressing a triple HA9 epitope endogenously tagged PLP1 failed to detect expression of Pf PLP1 during the blood stage [ 41 ]. Additionally, a deletion strain of Pf PLP1 ( Pf∆plp1 ) showed normal asexual growth when cultured in erythrocytes in vitro [ 41 ].…”

Section: Apicomplexans Share a Family Of Macpf Pfps That Function mentioning

confidence: 99%

“…However, studies with P. falciparum parasites expressing a triple HA9 epitope endogenously tagged PLP1 failed to detect expression of Pf PLP1 during the blood stage [ 41 ]. Additionally, a deletion strain of Pf PLP1 ( Pf∆plp1 ) showed normal asexual growth when cultured in erythrocytes in vitro [ 41 ]. Pf∆plp1 parasites also are not defective in a number of gametocytes, midgut oocysts, or salivary gland sporozoites.…”

Section: Apicomplexans Share a Family Of Macpf Pfps That Function mentioning

confidence: 99%

Structural Features of Apicomplexan Pore-Forming Proteins and Their Roles in Parasite Cell Traversal and Egress

Guerra

Carruthers

2017

Toxins

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Apicomplexan parasites cause diseases, including malaria and toxoplasmosis, in a range of hosts, including humans. These intracellular parasites utilize pore-forming proteins that disrupt host cell membranes to either traverse host cells while migrating through tissues or egress from the parasite-containing vacuole after replication. This review highlights recent insight gained from the newly available three-dimensional structures of several known or putative apicomplexan pore-forming proteins that contribute to cell traversal or egress. These new structural advances suggest that parasite pore-forming proteins use distinct mechanisms to disrupt host cell membranes at multiple steps in parasite life cycles. How proteolytic processing, secretion, environment, and the accessibility of lipid receptors regulate the membranolytic activities of such proteins is also discussed.

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“…Motility is essential for Plasmodium to properly navigate through both the host skin and hepatic microenvironments. Sporozoites utilize substrate-dependent gliding motility and cell traversal in both locations as they travel toward the host hepatocytes 5 – 13 . Within the skin, sporozoites are able to switch from an initial rapid motility to a more restricted movement around the dermal blood vessels 7 .…”

Section: Introductionmentioning

confidence: 99%

A mosquito salivary gland protein partially inhibits Plasmodium sporozoite cell traversal and transmission

et al. 2018

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The key step during the initiation of malaria is for motile Plasmodium parasites to exit the host dermis and infect the liver. During transmission, the parasites in the form of sporozoites, are injected together with mosquito saliva into the skin. However, the contribution of vector saliva to sporozoite activity during the establishment of the initial infection of the liver is poorly understood. Here we identify a vector protein by mass spectrometry, with similarity to the human gamma interferon inducible thiol reductase (GILT), that is associated with saliva sporozoites of infected Anopheles mosquitoes and has a negative impact on the speed and cell traversal activity of Plasmodium. This protein, referred to as mosquito GILT (mosGILT) represents an example of a protein found in mosquito saliva that may negatively influence sporozoite movement in the host and could lead to new approaches to prevent malaria.

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Molecular mechanisms of host cell traversal by malaria sporozoites

Cited by 18 publications

References 67 publications

Gliding motility of Plasmodium merozoites

Gliding motility of Plasmodium merozoites

Structural Features of Apicomplexan Pore-Forming Proteins and Their Roles in Parasite Cell Traversal and Egress

A mosquito salivary gland protein partially inhibits Plasmodium sporozoite cell traversal and transmission

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