Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus.
Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus.
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DOI:
10.1371/journal.ppat.1007043
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发表时间:
2018-05
期刊:
影响因子:
6.7
通讯作者:
Gibson W
中科院分区:
文献类型:
--
作者:
Peacock L;Kay C;Bailey M;Gibson W
Trypanosomatids such as Leishmania and Trypanosoma are digenetic, single-celled, parasitic flagellates that undergo complex life cycles involving morphological and metabolic changes to fit them for survival in different environments within their mammalian and insect hosts. According to current consensus, asymmetric division enables trypanosomatids to achieve the major morphological rearrangements associated with transition between developmental stages. Contrary to this view, here we show that the African trypanosome Trypanosoma congolense, an important livestock pathogen, undergoes extensive cell remodelling, involving shortening of the cell body and flagellum, during its transition from free-swimming proventricular forms to attached epimastigotes in vitro. Shortening of the flagellum was associated with accumulation of PFR1, a major constituent of the paraflagellar rod, in the mid-region of the flagellum where it was attached to the substrate. However, the PFR1 depot was not essential for attachment, as it accumulated several hours after initial attachment of proventricular trypanosomes. Detergent and CaCl2 treatment failed to dislodge attached parasites, demonstrating the robust nature of flagellar attachment to the substrate; the PFR1 depot was also unaffected by these treatments. Division of the remodelled proventricular trypanosome was asymmetric, producing a small daughter cell. Each mother cell went on to produce at least one more daughter cell, while the daughter trypanosomes also proliferated, eventually resulting in a dense culture of epimastigotes. Here, by observing the synchronous development of the homogeneous population of trypanosomes in the tsetse proventriculus, we have been able to examine the transition from proventricular forms to attached epimastigotes in detail in T. congolense. This transition is difficult to observe in vivo as it happens inside the mouthparts of the tsetse fly. In T. brucei, this transition is achieved by asymmetric division of long trypomastigotes in the proventriculus, yielding short epimastigotes, which go on to colonise the salivary glands. Thus, despite their close evolutionary relationship and shared developmental route within the vector, T. brucei and T. congolense have evolved different ways of accomplishing the same developmental transition from proventricular form to attached epimastigote. Tsetse-transmitted trypanosomes are parasitic protists that cause severe human and livestock diseases in tropical Africa. During their developmental cycle in the tsetse fly, these trypanosomes undergo complex cycles of differentiation and proliferation. Here we have investigated part of the developmental cycle of the major livestock pathogen Trypanosoma congolense as it moves from the fly midgut via the foregut to the mouthparts, where it reacquires infectivity to mammalian hosts. This transition is difficult to observe in vivo because of the small numbers of migratory trypanosomes and their inaccessibility in the fly. However, prior to migration, trypanosomes accumulate in the proventriculus, the valve that separates the foregut from the midgut, and we were able to observe the behaviour of these cells in vitro. On release from the proventriculus, these trypanosomes readily attach to a glass microscope slide and then undergo drastic remodelling to become short, stout cells, before each produces a small daughter cell. Each mother cell goes on to produce at least one further daughter trypanosome in the same way, while the daughter cells also proliferate as attached cells. We assume that these events would normally happen in vivo inside the tsetse proboscis. In T. brucei the equivalent developmental transition takes place in the proventriculus or foregut in free-swimming rather than attached cells, and is achieved via an asymmetric division. Thus, despite their close evolutionary relationship, these two trypanosome species have evolved different ways of accomplishing what is essentially the same developmental transition.
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影响因子:
7.8
作者:
Marshall, W F;Rosenbaum, J L
通讯作者:
Rosenbaum, J L
DOI:
10.1080/00034983.1947.11685305
发表时间:
1947-01-01
影响因子:
--
作者:
LEWIS, EA;LANGRIDGE, WP
通讯作者:
LANGRIDGE, WP
影响因子:
2.4
作者:
PRAIN, CJ;ROSS, CA
通讯作者:
ROSS, CA
影响因子:
11.8
作者:
Pan, JM;Snell, WJ
通讯作者:
Snell, WJ
影响因子:
2.4
作者:
MacLeod, E. T.;Maudlin, I.;Welburn, S. C.
通讯作者:
Welburn, S. C.