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Vital role for Plasmodium berghei Kinesin8B in axoneme assembly during male gamete formation and mosquito transmission.
Cell Microbiol 2019; :e13121CM

Abstract

Sexual development is an essential phase in the Plasmodium life cycle, where male gametogenesis is an unusual and extraordinarily rapid process. It produces 8 haploid motile microgametes, from a microgametocyte within 15 minutes. Its unique achievement lies in linking the assembly of 8 axonemes in the cytoplasm to the three rounds of intranuclear genome replication, forming motile microgametes, which are expelled in a process called exflagellation. Surprisingly little is known about the actors involved in these processes. We are interested in kinesins, molecular motors that could play potential roles in male gametogenesis. We have undertaken a functional characterization in Plasmodium berghei of kinesin-8B (PbKIN8B) expressed specifically in male gametocytes and gametes. By generating Pbkin8B-gfp parasites, we show that PbKIN8B is specifically expressed during male gametogenesis and is associated with the axoneme. We created a ΔPbkin8B knockout cell line and analysed the consequences of the absence of PbKIN8B on male gametogenesis. We show that the ability to produce sexually differentiated gametocytes is not affected in ΔPbkin8B parasites and that the 3 rounds of genome replication occur normally. Nevertheless, the development to free motile microgametes is halted and the life cycle is interrupted in vivo. Ultrastructural analysis revealed that intranuclear mitoses is unaffected whereas cytoplasmic microtubules, although assembled in doublets and elongated, fail to assemble in the normal axonemal "9+2" structure and become motile. Absence of a functional axoneme prevented microgamete assembly and release from the microgametocyte, severely reducing infection of the mosquito vector. This is the first functional study of a kinesin involved in male gametogenesis. These results reveal a previously unknown role for PbKIN8B in male gametogenesis, providing new insights into Plasmodium flagellar formation.

Authors+Show Affiliations

UMR 7245 CNRS Molécules de Communication et Adaptation des Micro-organismes, Muséum National d'Histoire Naturelle, Sorbonne Universités, Paris Cedex 05, France.Department of Life Sciences, Imperial College of London, London, United Kingdom.Nuffield Department of Clinical Laboratory Science, University of Oxford, Oxford, United Kingdom.UMR 7245 CNRS Molécules de Communication et Adaptation des Micro-organismes, Muséum National d'Histoire Naturelle, Sorbonne Universités, Paris Cedex 05, France.UMR 7245 CNRS Molécules de Communication et Adaptation des Micro-organismes, Muséum National d'Histoire Naturelle, Sorbonne Universités, Paris Cedex 05, France. Institute of Parasitology, Macdonald Campus, McGill University 21, Sainte-Anne-de-Bellevue, QC, Canada.Department of Life Sciences, Imperial College of London, London, United Kingdom.UMR 7245 CNRS Molécules de Communication et Adaptation des Micro-organismes, Muséum National d'Histoire Naturelle, Sorbonne Universités, Paris Cedex 05, France.UMR 7245 CNRS Molécules de Communication et Adaptation des Micro-organismes, Muséum National d'Histoire Naturelle, Sorbonne Universités, Paris Cedex 05, France.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31634979

Citation

Depoix, D, et al. "Vital Role for Plasmodium Berghei Kinesin8B in Axoneme Assembly During Male Gamete Formation and Mosquito Transmission." Cellular Microbiology, 2019, pp. e13121.
Depoix D, Marques SR, Ferguson DJP, et al. Vital role for Plasmodium berghei Kinesin8B in axoneme assembly during male gamete formation and mosquito transmission. Cell Microbiol. 2019.
Depoix, D., Marques, S. R., Ferguson, D. J. P., Chaouch, S., Duguet, T., Sinden, R. E., ... Kohl, L. (2019). Vital role for Plasmodium berghei Kinesin8B in axoneme assembly during male gamete formation and mosquito transmission. Cellular Microbiology, pp. e13121. doi:10.1111/cmi.13121.
Depoix D, et al. Vital Role for Plasmodium Berghei Kinesin8B in Axoneme Assembly During Male Gamete Formation and Mosquito Transmission. Cell Microbiol. 2019 Oct 21;e13121. PubMed PMID: 31634979.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Vital role for Plasmodium berghei Kinesin8B in axoneme assembly during male gamete formation and mosquito transmission. AU - Depoix,D, AU - Marques,S R, AU - Ferguson,D J P, AU - Chaouch,S, AU - Duguet,T, AU - Sinden,R E, AU - Grellier,P, AU - Kohl,L, Y1 - 2019/10/21/ PY - 2019/06/08/received PY - 2019/08/02/revised PY - 2019/09/23/accepted PY - 2019/10/22/entrez PY - 2019/10/22/pubmed PY - 2019/10/22/medline SP - e13121 EP - e13121 JF - Cellular microbiology JO - Cell. Microbiol. N2 - Sexual development is an essential phase in the Plasmodium life cycle, where male gametogenesis is an unusual and extraordinarily rapid process. It produces 8 haploid motile microgametes, from a microgametocyte within 15 minutes. Its unique achievement lies in linking the assembly of 8 axonemes in the cytoplasm to the three rounds of intranuclear genome replication, forming motile microgametes, which are expelled in a process called exflagellation. Surprisingly little is known about the actors involved in these processes. We are interested in kinesins, molecular motors that could play potential roles in male gametogenesis. We have undertaken a functional characterization in Plasmodium berghei of kinesin-8B (PbKIN8B) expressed specifically in male gametocytes and gametes. By generating Pbkin8B-gfp parasites, we show that PbKIN8B is specifically expressed during male gametogenesis and is associated with the axoneme. We created a ΔPbkin8B knockout cell line and analysed the consequences of the absence of PbKIN8B on male gametogenesis. We show that the ability to produce sexually differentiated gametocytes is not affected in ΔPbkin8B parasites and that the 3 rounds of genome replication occur normally. Nevertheless, the development to free motile microgametes is halted and the life cycle is interrupted in vivo. Ultrastructural analysis revealed that intranuclear mitoses is unaffected whereas cytoplasmic microtubules, although assembled in doublets and elongated, fail to assemble in the normal axonemal "9+2" structure and become motile. Absence of a functional axoneme prevented microgamete assembly and release from the microgametocyte, severely reducing infection of the mosquito vector. This is the first functional study of a kinesin involved in male gametogenesis. These results reveal a previously unknown role for PbKIN8B in male gametogenesis, providing new insights into Plasmodium flagellar formation. SN - 1462-5822 UR - https://www.unboundmedicine.com/medline/citation/31634979/Vital_role_for_Plasmodium_berghei_Kinesin8B_in_axoneme_assembly_during_male_gamete_formation_and_mosquito_transmission L2 - https://doi.org/10.1111/cmi.13121 DB - PRIME DP - Unbound Medicine ER -