Role of Plasmodium Berghei Ookinete Surface and Oocyst Capsule Protein, a Novel Oocyst Capsule-associated Protein, in Ookinete Motility

Overview

Journal Parasit Vectors

Publisher Biomed Central

Specialties Parasitology
Tropical Medicine

Date 2021 Jul 22

PMID 34289894

Citations 6

Authors

Kazuhiko Nakayama

Yuta Kimura

Yu Kitahara

Akira Soga

Asako Haraguchi

Jun Hakozaki

Makoto Sugiyama

Kodai Kusakisako

Shinya Fukumoto

Hiromi Ikadai

Affiliations

Soon will be listed here.

Abstract

Background: Plasmodium sp., which causes malaria, must first develop in mosquitoes before being transmitted. Upon ingesting infected blood, gametes form in the mosquito lumen, followed by fertilization and differentiation of the resulting zygotes into motile ookinetes. Within 24 h of blood ingestion, these ookinetes traverse mosquito epithelial cells and lodge below the midgut basal lamina, where they differentiate into sessile oocysts that are protected by a capsule.

Methods: We identified an ookinete surface and oocyst capsule protein (OSCP) that is involved in ookinete motility as well as oocyst capsule formation.

Results: We found that knockout of OSCP in parasite decreases ookinete gliding motility and gradually reduces the number of oocysts. On day 15 after blood ingestion, the oocyst wall was significantly thinner. Moreover, adding anti-OSCP antibodies decreased the gliding speed of wild-type ookinetes in vitro. Adding anti-OSCP antibodies to an infected blood meal also resulted in decreased oocyst formation.

Conclusion: These findings may be useful for the development of a transmission-blocking tool for malaria.

Citing Articles

The C-terminal region of the Plasmodium berghei gamete surface 184-kDa protein Pb184 contributes to fertilization and male gamete binding to the residual body.

Nakayama K, Haraguchi A, Hakozaki J, Nakamura S, Kusakisako K, Ikadai H Parasit Vectors. 2024; 17(1):304.

PMID: 39003498 PMC: 11246575. DOI: 10.1186/s13071-024-06374-7.

Mosquito midgut stem cell cellular defense response limits Plasmodium parasite infection.

Barletta A, Smith J, Burkart E, Bondarenko S, Sharakhov I, Criscione F Nat Commun. 2024; 15(1):1422.

PMID: 38365823 PMC: 10873411. DOI: 10.1038/s41467-024-45550-2.

Plasmodium sporozoite excystation involves local breakdown of the oocyst capsule.

Saeed S, Tremp A, Dessens J Sci Rep. 2023; 13(1):22222.

PMID: 38097730 PMC: 10721906. DOI: 10.1038/s41598-023-49442-1.

Formation of free oocysts in Anopheles mosquitoes injected with Plasmodium ookinetes.

Haraguchi A, Takano M, Hakozaki J, Nakayama K, Nakamura S, Yoshikawa Y J Vet Med Sci. 2023; 85(9):921-928.

PMID: 37407494 PMC: 10539829. DOI: 10.1292/jvms.23-0099.

Escaping the enemy's bullets: an update on how malaria parasites evade host immune response.

Ezema C, Okagu I, Chidike Ezeorba T Parasitol Res. 2023; 122(8):1715-1731.

PMID: 37219610 PMC: 10348937. DOI: 10.1007/s00436-023-07868-6.

References

Bennink S, Kiesow M, Pradel G . The development of malaria parasites in the mosquito midgut. Cell Microbiol. 2016; 18(7):905-18. PMC: 5089571. DOI: 10.1111/cmi.12604. View

Smith R, Vega-Rodriguez J, Jacobs-Lorena M . The Plasmodium bottleneck: malaria parasite losses in the mosquito vector. Mem Inst Oswaldo Cruz. 2014; 109(5):644-61. PMC: 4156458. View

Ghosh A, Edwards M, Jacobs-Lorena M . The journey of the malaria parasite in the mosquito: hopes for the new century. Parasitol Today. 2000; 16(5):196-201. DOI: 10.1016/s0169-4758(99)01626-9. View

Han Y, Thompson J, Kafatos F . Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J. 2000; 19(22):6030-40. PMC: 305834. DOI: 10.1093/emboj/19.22.6030. View

Kumar S, Barillas-Mury C . Ookinete-induced midgut peroxidases detonate the time bomb in anopheline mosquitoes. Insect Biochem Mol Biol. 2005; 35(7):721-7. DOI: 10.1016/j.ibmb.2005.02.014. View

Liu F, Li L, Zheng W, He Y, Wang Y, Zhu X . Characterization of Plasmodium berghei Pbg37 as Both a Pre- and Postfertilization Antigen with Transmission-Blocking Potential. Infect Immun. 2018; 86(8). PMC: 6056874. DOI: 10.1128/IAI.00785-17. View

Tomas A, Margos G, Dimopoulos G, van Lin L, Sinha R, Lupetti P . P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 2001; 20(15):3975-83. PMC: 149139. DOI: 10.1093/emboj/20.15.3975. View

Ukegbu C, Akinosoglou K, Christophides G, Vlachou D . Plasmodium berghei PIMMS2 Promotes Ookinete Invasion of the Anopheles gambiae Mosquito Midgut. Infect Immun. 2017; 85(8). PMC: 5520436. DOI: 10.1128/IAI.00139-17. View

Ukegbu C, Giorgalli M, Tapanelli S, Rona L, Jaye A, Wyer C . PIMMS43 is required for malaria parasite immune evasion and sporogonic development in the mosquito vector. Proc Natl Acad Sci U S A. 2020; 117(13):7363-7373. PMC: 7132314. DOI: 10.1073/pnas.1919709117. View

10.

Ukegbu C, Giorgalli M, Yassine H, Ramirez J, Taxiarchi C, Barillas-Mury C . Plasmodium berghei P47 is essential for ookinete protection from the Anopheles gambiae complement-like response. Sci Rep. 2017; 7(1):6026. PMC: 5519742. DOI: 10.1038/s41598-017-05917-6. View

11.

Deligianni E, de Monerri N, McMillan P, Bertuccini L, Superti F, Manola M . Essential role of Plasmodium perforin-like protein 4 in ookinete midgut passage. PLoS One. 2018; 13(8):e0201651. PMC: 6089593. DOI: 10.1371/journal.pone.0201651. View

12.

Dessens J, Beetsma A, Dimopoulos G, Wengelnik K, Crisanti A, Kafatos F . CTRP is essential for mosquito infection by malaria ookinetes. EMBO J. 1999; 18(22):6221-7. PMC: 1171685. DOI: 10.1093/emboj/18.22.6221. View

13.

Dessens J, Mendoza J, Claudianos C, Vinetz J, Khater E, Hassard S . Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect Immun. 2001; 69(6):4041-7. PMC: 98467. DOI: 10.1128/IAI.69.6.4041-4047.2001. View

14.

Dessens J, Siden-Kiamos I, Mendoza J, Mahairaki V, Khater E, Vlachou D . SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol. 2003; 49(2):319-29. DOI: 10.1046/j.1365-2958.2003.03566.x. View

15.

Ecker A, Pinto S, Baker K, Kafatos F, Sinden R . Plasmodium berghei: plasmodium perforin-like protein 5 is required for mosquito midgut invasion in Anopheles stephensi. Exp Parasitol. 2007; 116(4):504-8. PMC: 1916484. DOI: 10.1016/j.exppara.2007.01.015. View

16.

Kadota K, Ishino T, Matsuyama T, Chinzei Y, Yuda M . Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci U S A. 2004; 101(46):16310-5. PMC: 524694. DOI: 10.1073/pnas.0406187101. View

17.

Kaneko I, Iwanaga S, Kato T, Kobayashi I, Yuda M . Genome-Wide Identification of the Target Genes of AP2-O, a Plasmodium AP2-Family Transcription Factor. PLoS Pathog. 2015; 11(5):e1004905. PMC: 4446032. DOI: 10.1371/journal.ppat.1004905. View

18.

Kariu T, Ishino T, Yano K, Chinzei Y, Yuda M . CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol. 2006; 59(5):1369-79. DOI: 10.1111/j.1365-2958.2005.05024.x. View

19.

Tsai Y, Hayward R, Langer R, Fidock D, Vinetz J . Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect Immun. 2001; 69(6):4048-54. PMC: 98468. DOI: 10.1128/IAI.69.6.4048-4054.2001. View

20.

Yuda M, Sakaida H, Chinzei Y . Targeted disruption of the plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito. J Exp Med. 1999; 190(11):1711-6. PMC: 2195737. DOI: 10.1084/jem.190.11.1711. View