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Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion.
Cell Microbiol. 2004 Jul; 6(7):671-85.CM

Abstract

Invasion of the Anopheles mosquito midgut by the Plasmodium ookinete is a critical step in the malaria transmission cycle. We have generated a fluorescent P. berghei transgenic line that expresses GFP in the ookinete and oocyst stages, and used it to perform the first real-time analysis of midgut invasion in the living mosquito as well as in explanted intact midguts whose basolateral plasma membranes were vitally stained. These studies permitted detailed analysis of parasite motile behaviour in the midgut and cell biological analysis of the invasion process. Throughout its journey, the ookinete displays distinct modes of motility: stationary rotation, translocational spiralling and straight-segment motility. Spiralling is based on rotational motility combined with translocation steps and changes in direction, which are achieved by transient attachments of the ookinete's trailing end. As it moves from the apical to the basal side of the midgut epithelium, the ookinete uses a predominant intracellular route and appears to glide on the membrane in foldings of the basolateral domain. However, it traverses serially the cytoplasm of several midgut cells before entering and migrating through the basolateral intercellular space to access the basal lamina. The invaded cells commit apoptosis, and their expulsion from the epithelium invokes wound repair mechanisms including extensive lamellipodia crawling. A 'hood' of lamellipodial origin, provided by the invaded cell, covers the ookinete during its egress from the epithelium. The flexible ookinete undergoes shape changes and temporary constrictions associated with passage through the plasma membranes. Similar observations were made in both A. gambiae and A. stephensi, demonstrating the conservation of P. berghei interactions with these vectors.

Authors+Show Affiliations

European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

15186403

Citation

Vlachou, Dina, et al. "Real-time, in Vivo Analysis of Malaria Ookinete Locomotion and Mosquito Midgut Invasion." Cellular Microbiology, vol. 6, no. 7, 2004, pp. 671-85.
Vlachou D, Zimmermann T, Cantera R, et al. Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol. 2004;6(7):671-85.
Vlachou, D., Zimmermann, T., Cantera, R., Janse, C. J., Waters, A. P., & Kafatos, F. C. (2004). Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cellular Microbiology, 6(7), 671-85.
Vlachou D, et al. Real-time, in Vivo Analysis of Malaria Ookinete Locomotion and Mosquito Midgut Invasion. Cell Microbiol. 2004;6(7):671-85. PubMed PMID: 15186403.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. AU - Vlachou,Dina, AU - Zimmermann,Timo, AU - Cantera,Rafael, AU - Janse,Chris J, AU - Waters,Andrew P, AU - Kafatos,Fotis C, PY - 2004/6/10/pubmed PY - 2004/7/16/medline PY - 2004/6/10/entrez SP - 671 EP - 85 JF - Cellular microbiology JO - Cell. Microbiol. VL - 6 IS - 7 N2 - Invasion of the Anopheles mosquito midgut by the Plasmodium ookinete is a critical step in the malaria transmission cycle. We have generated a fluorescent P. berghei transgenic line that expresses GFP in the ookinete and oocyst stages, and used it to perform the first real-time analysis of midgut invasion in the living mosquito as well as in explanted intact midguts whose basolateral plasma membranes were vitally stained. These studies permitted detailed analysis of parasite motile behaviour in the midgut and cell biological analysis of the invasion process. Throughout its journey, the ookinete displays distinct modes of motility: stationary rotation, translocational spiralling and straight-segment motility. Spiralling is based on rotational motility combined with translocation steps and changes in direction, which are achieved by transient attachments of the ookinete's trailing end. As it moves from the apical to the basal side of the midgut epithelium, the ookinete uses a predominant intracellular route and appears to glide on the membrane in foldings of the basolateral domain. However, it traverses serially the cytoplasm of several midgut cells before entering and migrating through the basolateral intercellular space to access the basal lamina. The invaded cells commit apoptosis, and their expulsion from the epithelium invokes wound repair mechanisms including extensive lamellipodia crawling. A 'hood' of lamellipodial origin, provided by the invaded cell, covers the ookinete during its egress from the epithelium. The flexible ookinete undergoes shape changes and temporary constrictions associated with passage through the plasma membranes. Similar observations were made in both A. gambiae and A. stephensi, demonstrating the conservation of P. berghei interactions with these vectors. SN - 1462-5814 UR - https://www.unboundmedicine.com/medline/citation/15186403/Real_time_in_vivo_analysis_of_malaria_ookinete_locomotion_and_mosquito_midgut_invasion_ L2 - https://onlinelibrary.wiley.com/resolve/openurl?genre=article&sid=nlm:pubmed&issn=1462-5814&date=2004&volume=6&issue=7&spage=671 DB - PRIME DP - Unbound Medicine ER -