Important Extracellular Interactions Between Plasmodium Sporozoites and Host Cells Required for Infection

Overview

Journal Trends Parasitol

Specialty Parasitology

Date 2018 Dec 26

PMID 30583849

Citations 16

Authors

Kirsten Dundas

Melanie J Shears

Photini Sinnis

Gavin J Wright

Affiliations

Soon will be listed here.

Abstract

Malaria is an infectious disease, caused by Plasmodium parasites, that remains a major global health problem. Infection begins when salivary gland sporozoites are transmitted through the bite of an infected mosquito. Once within the host, sporozoites navigate through the dermis, into the bloodstream, and eventually invade hepatocytes. While we have an increasingly sophisticated cellular description of this journey, our molecular understanding of the extracellular interactions between the sporozoite and mammalian host that regulate migration and invasion remain comparatively poor. Here, we review the current state of our understanding, highlight the technical limitations that have frustrated progress, and outline how new approaches will help to address this knowledge gap with the ultimate aim of improving malaria treatments.

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References

Kudryashev M, Munter S, Lemgruber L, Montagna G, Stahlberg H, Matuschewski K . Structural basis for chirality and directional motility of Plasmodium sporozoites. Cell Microbiol. 2012; 14(11):1757-68. PMC: 4116596. DOI: 10.1111/j.1462-5822.2012.01836.x. View

Ferguson D, Balaban A, Patzewitz E, Wall R, Hopp C, Poulin B . The repeat region of the circumsporozoite protein is critical for sporozoite formation and maturation in Plasmodium. PLoS One. 2014; 9(12):e113923. PMC: 4250072. DOI: 10.1371/journal.pone.0113923. View

Jimah J, Salinas N, Sala-Rabanal M, Jones N, Sibley L, Nichols C . Malaria parasite CelTOS targets the inner leaflet of cell membranes for pore-dependent disruption. Elife. 2016; 5. PMC: 5132341. DOI: 10.7554/eLife.20621. View

Dundas K, Shears M, Sun Y, Hopp C, Crosnier C, Metcalf T . Alpha-v-containing integrins are host receptors for the sporozoite surface protein, TRAP. Proc Natl Acad Sci U S A. 2018; 115(17):4477-4482. PMC: 5924908. DOI: 10.1073/pnas.1719660115. View

Doud M, Koksal A, Mi L, Song G, Lu C, Springer T . Unexpected fold in the circumsporozoite protein target of malaria vaccines. Proc Natl Acad Sci U S A. 2012; 109(20):7817-22. PMC: 3356675. DOI: 10.1073/pnas.1205737109. View

Giovannini D, Spath S, Lacroix C, Perazzi A, Bargieri D, Lagal V . Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by apicomplexa. Cell Host Microbe. 2011; 10(6):591-602. DOI: 10.1016/j.chom.2011.10.012. View

Myung J, Marshall P, Sinnis P . The Plasmodium circumsporozoite protein is involved in mosquito salivary gland invasion by sporozoites. Mol Biochem Parasitol. 2003; 133(1):53-9. DOI: 10.1016/j.molbiopara.2003.09.002. View

Zimmerman B, Kelly B, McMillan B, Seegar T, Dror R, Kruse A . Crystal Structure of a Full-Length Human Tetraspanin Reveals a Cholesterol-Binding Pocket. Cell. 2016; 167(4):1041-1051.e11. PMC: 5127602. DOI: 10.1016/j.cell.2016.09.056. View

Armistead J, Wilson I, van Kuppevelt T, Dinglasan R . A role for heparan sulfate proteoglycans in Plasmodium falciparum sporozoite invasion of anopheline mosquito salivary glands. Biochem J. 2011; 438(3):475-83. PMC: 3173866. DOI: 10.1042/BJ20110694. View

10.

Kappe S, Bruderer T, Gantt S, Fujioka H, NUSSENZWEIG V, Menard R . Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J Cell Biol. 1999; 147(5):937-44. PMC: 2169348. DOI: 10.1083/jcb.147.5.937. View

11.

Combe A, Moreira C, Ackerman S, Thiberge S, Templeton T, Menard R . TREP, a novel protein necessary for gliding motility of the malaria sporozoite. Int J Parasitol. 2008; 39(4):489-96. DOI: 10.1016/j.ijpara.2008.10.004. View

12.

Risco-Castillo V, Topcu S, Marinach C, Manzoni G, Bigorgne A, Briquet S . Malaria Sporozoites Traverse Host Cells within Transient Vacuoles. Cell Host Microbe. 2015; 18(5):593-603. DOI: 10.1016/j.chom.2015.10.006. View

13.

Menard R, Sultan A, Cortes C, Altszuler R, van Dijk M, Janse C . Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature. 1997; 385(6614):336-40. DOI: 10.1038/385336a0. View

14.

Rodrigues C, Hannus M, Prudencio M, Martin C, Goncalves L, Portugal S . Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe. 2008; 4(3):271-82. DOI: 10.1016/j.chom.2008.07.012. View

15.

Sinnis P, Zavala F . The skin: where malaria infection and the host immune response begin. Semin Immunopathol. 2012; 34(6):787-92. PMC: 3934925. DOI: 10.1007/s00281-012-0345-5. View

16.

Frevert U, Sinnis P, Esko J, NUSSENZWEIG V . Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei sporozoite invasion in vitro. Mol Biochem Parasitol. 1996; 76(1-2):257-66. DOI: 10.1016/0166-6851(95)02563-4. View

17.

Ancsin J, Kisilevsky R . A binding site for highly sulfated heparan sulfate is identified in the N terminus of the circumsporozoite protein: significance for malarial sporozoite attachment to hepatocytes. J Biol Chem. 2004; 279(21):21824-32. DOI: 10.1074/jbc.M401979200. View

18.

Risco-Castillo V, Topcu S, Son O, Briquet S, Manzoni G, Silvie O . CD81 is required for rhoptry discharge during host cell invasion by Plasmodium yoelii sporozoites. Cell Microbiol. 2014; 16(10):1533-48. DOI: 10.1111/cmi.12309. View

19.

VanBuskirk K, ONeill M, De La Vega P, Maier A, Krzych U, Williams J . Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc Natl Acad Sci U S A. 2009; 106(31):13004-9. PMC: 2714279. DOI: 10.1073/pnas.0906387106. View

20.

Ejigiri I, Ragheb D, Pino P, Coppi A, Bennett B, Soldati-Favre D . Shedding of TRAP by a rhomboid protease from the malaria sporozoite surface is essential for gliding motility and sporozoite infectivity. PLoS Pathog. 2012; 8(7):e1002725. PMC: 3406075. DOI: 10.1371/journal.ppat.1002725. View