The Plasmodium alveolin IMC1a is stabilised by its terminal cysteine motifs and facilitates sporozoite morphogenesis and infectivity in a dose-dependent manner

Al-Khattaf, Fatimah S.; Tremp, Annie Z.; El-Houderi, Amira; Dessens, Johannes T.

doi:10.1016/j.molbiopara.2016.09.004

Cited by 11 publications

(15 citation statements)

References 33 publications

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“…Plasmodium encodes only eight alveolins with nonredundant roles at specific life cycle stages. Careful dissection of these proteins in Plasmodium berghei has shown that the composition of the SPN has a stage-specific role in maintaining the tensile strength of the parasite, as well as a role in morphology [60,85,87,92]. In both T. gondii and Sarcocystis, IMC proteins undergo a dynamic and hierarchical assembly throughout both endodyogeny and the life cycle [11,16].…”

Section: Stress-resistant Scaffoldingmentioning

confidence: 99%

The Riveting Cellular Structures of Apicomplexan Parasites

Harding

Frischknecht

2020

Trends in Parasitology

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Section: Stress-resistant Scaffoldingmentioning

confidence: 99%

The Riveting Cellular Structures of Apicomplexan Parasites

Harding

Frischknecht

2020

Trends in Parasitology

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“…These observations indicate that IMC1h without its non-alveolin module causes an intermediate phenotype with regards to sporozoite morphogenesis. Interestingly, mutations of putative amino- or carboxy-terminal palmitoylation sites of the sporozoite-specific alveolin IMC1a have also been shown to affect sporozoite shape and size, being in between that of null mutant and wildtype sporozoites (Al-Khattaf et al, 2017). Collectively, these findings point to a fundamental role of the alveolins in determining sporozoite size and shape.…”

Section: Discussionmentioning

confidence: 99%

Distinct Functional Contributions by the Conserved Domains of the Malaria Parasite Alveolin IMC1h

Coghlan

Tremp

Saeed

et al. 2019

Front. Cell. Infect. Microbiol.

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Invasive, motile life cycle stages (zoites) of apicomplexan parasites possess a cortical membrane skeleton composed of intermediate filaments with roles in zoite morphogenesis, tensile strength and motility. Its building blocks include a family of proteins called alveolins that are characterized by conserved “alveolin” domains composed of tandem repeat sequences. A subset of alveolins possess additional conserved domains that are structurally unrelated and the roles of which remain unclear. In this structure-function analysis we investigated the functional contributions of the “alveolin” vs. “non-alveolin” domains of IMC1h, a protein expressed in the ookinete and sporozoite life cycle stages of malaria parasites and essential for parasite transmission. Using allelic replacement in Plasmodium berghei , we show that the alveolin domain is responsible for targeting IMC1h to the membrane skeleton and, consequently, its deletion from the protein results in loss of function manifested by abnormally-shaped ookinetes and sporozoites with reduced tensile strength, motility and infectivity. Conversely, IMC1h lacking its non-alveolin conserved domain is correctly targeted and can facilitate tensile strength but not motility. Our findings support the concept that the alveolin module contains the properties for filament formation, and show for the first time that tensile strength makes an important contribution to zoite infectivity. The data furthermore provide new insight into the underlying molecular mechanisms of motility, indicating that tensile strength is mechanistically uncoupled from locomotion, and pointing to a role of the non-alveolin domain in the motility-enhancing properties of IMC1h possibly by engaging with the locomotion apparatus.

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“…2 and Text S1 to S7 ), and in some cases (e.g., Symbiodinium [ Text S5.24 ], Guillardia [ Text S4.43 ], and Toxoplasma [ Text S1.45 ]) they are abundant. Mutagenesis of the C residues in the IMC1c protein of Plasmodium affects sporozoite shape and infectivity ( 62 ), and the residues have been shown to undergo palmitoylation ( 173 ), possibly contributing to membrane associations.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, the only intermediate-filament proteins reported to form a membrane skeleton are the nuclear lamins ( 59 ). Therefore, referring to epiplastins as intermediate filaments or intermediate filament-like ( 24 , 27 , 32 , 36 , 51 , 60 – 62 ) can be misleading. Rather, the epiplastins represent a novel protein class that proves to be restricted, with a few interesting exceptions, to lineages that assemble epiplasts, a restriction that may be informative in assigning evolutionary relationships between various taxa.…”

Section: Introductionmentioning

confidence: 99%

Epiplasts: Membrane Skeletons and Epiplastin Proteins in Euglenids, Glaucophytes, Cryptophytes, Ciliates, Dinoflagellates, and Apicomplexans

Goodenough

Roth

Kariyawasam

et al. 2018

mBio

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Membrane skeletons associate with the inner surface of the plasma membrane to provide support for the fragile lipid bilayer and an elastic framework for the cell itself. Several radiations, including animals, organize such skeletons using actin/spectrin proteins, but four major radiations of eukaryotic unicellular organisms, including disease-causing parasites such as Plasmodium, have been known to construct an alternative and essential skeleton (the epiplast) using a class of proteins that we term epiplastins. We have identified epiplastins in two additional radiations and present images of their epiplasts using electron microscopy. We analyze the sequences and secondary structure of 219 epiplastins and present an in-depth overview and analysis of their known and posited roles in cellular organization and parasite infection. An understanding of epiplast assembly may suggest therapeutic approaches to combat infectious agents such as Plasmodium as well as approaches to the engineering of useful viscoelastic biofilms.

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The Plasmodium alveolin IMC1a is stabilised by its terminal cysteine motifs and facilitates sporozoite morphogenesis and infectivity in a dose-dependent manner

Abstract: Graphical abstract

Cited by 11 publications

References 33 publications

The Riveting Cellular Structures of Apicomplexan Parasites

The Riveting Cellular Structures of Apicomplexan Parasites

Distinct Functional Contributions by the Conserved Domains of the Malaria Parasite Alveolin IMC1h

Epiplasts: Membrane Skeletons and Epiplastin Proteins in Euglenids, Glaucophytes, Cryptophytes, Ciliates, Dinoflagellates, and Apicomplexans

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