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A more recent version of this article appeared on October 21, 2005
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M507511200v1
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Papers In Press, published online ahead of print August 22, 2005
J. Biol. Chem, 10.1074/jbc.M507511200
Submitted on July 11, 2005
Revised on August 19, 2005
Accepted on August 19, 2005

Distinct 3'untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania

François McNicoll, Michaela Müller, Serge Cloutier, Nathalie Boilard, Annie Rochette, Marthe Dubé, and Barbara Papadopoulou

Department of Medical Biology, Laval University, Quebec, Québec G1V 4G2

Corresponding Author: barbara.papadopoulou{at}crchul.ulaval.ca

We recently characterized a large developmentally regulated gene family in Leishmania encoding the amastin surface proteins. While studying the regulation of these genes, we identified a region of 770 nt within the 2055 nt 3'-untranslated region (3'UTR) that regulates stage-specific gene expression at the level of translation. An intriguing feature of this 3'UTR regulatory region is the presence of a ~450 nt element that is highly conserved among several Leishmania mRNAs. Here we show, using a luciferase reporter system and polysome profiling experiments, that the 450 nt element stimulates translation initiation of the amastin mRNA in response to heat shock, which is the main environmental change that the parasite encounters upon its entry into the mammalian host. Deletional analyses depicted a second region of ~100 nucleotides located at the 3'-end of several amastin transcripts which also activates translation in response to elevated temperature. Both 3'UTR regulatory elements act in an additive manner to stimulate amastin mRNA translation. In addition, we show that acidic pH encountered in the phagolysosomes of macrophages, the location of parasitic differentiation, triggers the accumulation of amastin transcripts by a distinct mechanism that is independent of the 450 nt and 100 nt elements. Overall, these important findings support that stage-specific posttranscriptional regulation of the amastin mRNAs in Leishmania is complex and involves the coordination of distinct mechanisms controlling mRNA stability and translation that are independently triggered by key environmental signals inducing parasite’s differentiation within macrophages.


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